Novitatesamerican MUSEUM PUBLISHED by the AMERICAN MUSEUM of NATURAL HISTORY CENTRAL PARK WEST at 79TH STREET, NEW YORK, N.Y

Home , Desman

NovitatesAMERICAN MUSEUM PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY CENTRAL PARK WEST AT 79TH STREET, NEW YORK, N.Y. 10024 Number 3103, 54 pp., 8 figures, 5 tables June 24, 1994

The Case for Chiropteran Monophyly

NANCY B. SIMMONS'

CONTENTS Abstract ...... 2 Introduction ...... 2 Microchiroptera and Megachiroptera ...... 2 Origins of the Bat Monophyly Controversy ...... 3 Review of Phylogenetic Studies ...... 4 Taxonomic Sampling ...... 5 Results of Biochemical and Molecular Studies ...... 6 Results of Morphological Studies ...... 13 Results of Studies Combining Morphological and Molecular Data ...... 18 Summary ...... 18 Morphological Characters Supporting Bat Monophyly ...... 19 Dentition ...... 19 Skull and Cranial Vascular System ...... 20 Postcranial Musculoskeletal System ...... 24 Fetal Membranes ...... 34 Nervous System ...... 37 Rejected Putative Synapomorphies ...... 38 Discussion and Conclusions ...... 42 What is the Sister Group of Bats? ...... 42 Directions for Future Research ...... 44 Acknowledgments ...... 46 References ...... 46

' Assistant Curator, Department of Mammalogy, American Museum of Natural History.

ABSTRACT The current controversy concerning bat mono- rRNA gene, and cytochrome oxidase subunit II phyly centers on relationships ofMicrochiroptera, gene). In no instance have molecular data provid- Megachiroptera, Primates, and several other groups ed unambiguous support for bat diphyly. Mor- ofmammals. Despite claims to the contrary, stud- phological data show a slightly different pattern. ies of both molecular and morphological data Neural and penial characters support diphyly of strongly support bat monophyly and a single origin bats, but other data subsets clearly support bat for powered flight in mammals. Analyses of some monophyly (e.g., characters of the cranium and molecular data sets have yielded inconclusive re- postcranial skeleton, vascular system, muscles, and sults (e.g., rDNA restriction sites, aA-crystallin fetal membranes). When all of the morphological amino acid sequences, and cytochrome oxidase data are considered together, the combined data subunit I gene nucleotide sequences). However, set strongly supports bat monophyly. Over 25 analyses of most biochemical and molecular data morphological synapomorphies-many of which support monophyly of bats (e.g., albumin im- consist of complex suites of modifications-di- munological distances, DNA-DNA hybridization, agnose the monophyletic order Chiroptera. The a-globin + 0-globin amino acid sequences, nucle- fact that these synapomorphies represent many otide sequence data from the e-globin gene, inter- different anatomical systems further strengthens photoreceptor retinoid binding protein gene, 12S the case for chiropteran monophyly.

INTRODUCTION

Monophyly ofChiroptera -and a single or- ing several significant molecular studies. As igin for powered flight in mammals-has been a result, the controversy remained largely un- assumed by most evolutionary biologists be- resolved. However, since that time over a cause all bats apparently share a unique set dozen new phylogenetic studies have been of specializations for flight. However, bat published (tables 1, 2, 3), and the data sup- monophyly and homology ofthe chiropteran porting different phylogenetic hypotheses wing have been questioned by authors who have been further critiqued (e.g., Thiele et have suggested that Megachiroptera and Mi- al., 1991; Johnson and Kirsch, 1993; Kaas crochiroptera may not be sister taxa (Jones and Preuss, 1993; Simmons, 1993). These and Genoways, 1970; Smith, 1976, 1980; studies have added considerably to our Smith and Madkour, 1980; Hill and Smith, knowledge and understanding ofrelevant data 1984; Pettigrew, 1986, 1991a, 1991b; Petti- and methodological issues, and have set the grew and Jamieson, 1987; Pettigrew et al., stage for resolution of the debate. 1989). If the two major bat lineages are only distantly related and their most recent common ancestor was nonvolant, then a dual or- MICROCHIROPTERA AND MEGACHIROPTERA igin for wings and powered flight within In any phylogenetic argument it is impor- Mammalia must be hypothesized. tant that the taxa under consideration (the Bat diphyly and related hypotheses (e.g., "operational taxonomic units") be mono- megachiropterans as "flying primates") have phyletic. One aspect of bat systematics that been the focus ofintense discussion in recent has not been the source of controversy is the years, with some authors defending the tra- status ofthe two bat suborders -there is gen- ditional concept of a monophyletic Chirop- eral agreement that Megachiroptera and Mi- tera (e.g., Wible and Novacek, 1988) while crochiroptera are each monophyletic taxa others supported bat diphyly (e.g., Pettigrew (Smith, 1976, 1980; Van Valen, 1979; No- et al., 1989). In 1991 the controversy was vacek, 1980b, 1987; Pettigrew et al., 1989; reviewed in a series of papers that appeared Pettigrew, 1991a, 1991b; Baker et al., 1991a, together in Systematic Zoology (i.e., Baker et 1991b; Kay et al., 1992; Beard, 1993a). al., 1991b; Pettigrew, 1991a, 1991b; Sim- Monophyly of Microchiroptera has rarely mons et al., 1991). At that time, much ofthe been questioned because all members of the relevant data remained unpublished, includ- group share a unique system of laryngeal 1994 SIMMONS: CHIROPTERAN MONOPHYLY 3 echolocation (Fleischer, 1973, 1978; Hill and orous-type dentition (Revilliod, 1922; Rus- Smith, 1984; Novacek, 1987; Pettigrew et al., sell and Sige, 1970; Slaughter, 1970). Nev- 1989). Many cetaceans also use sophisticated ertheless, Archaeopteropus is widely regarded echolocation, but the anatomical basis ofthe to be a megachiropteran because of similar- system is quite different (Fleischer, 1973, ities in wing morphology shared by this taxon 1978). In addition to features related to echo- and extant megachiropterans (Anderson, location, all microchiropterans share a unique 1912; Revilliod, 1922; Dal Piaz, 1937; Ha- arrangement of the gray matter in the spinal bersetzer and Storch, 1987). cord plus several apomorphic features of the Consideration ofthe fossil record indicates cranium and postcranium (Van Valen, 1979; that the lineages leading to extant megachi- Novacek, 1987; Pettigrew et al., 1989; Kay ropterans and microchiropterans have been et al., 1992; Beard, 1993a). separated since at least the Late Eocene, over Megachiroptera also appears to be mono- 50 million years. During this time a great deal phyletic. Extant megachiropterans share den- ofmolecular and morphological evolution has tal specializations associated with frugivory taken place, complicating efforts to resolve (Slaughter, 1970; Koopman and Maclntyre, higher-level relationships (Baker et al., 199 la, 1980), an unusual bilobed keel on the ma- 199 ib). Many significant morphological, be- nubrium (personal obs.), and sperm with sev- havioral, and genetic differences exist be- eral unique structural features (Rouse and tween Megachiroptera and Microchiroptera Robson, 1986). In addition, the nutrient sys- (Jones and Genoways, 1970; Pettigrew et al., tem of the megachiropteran retina involves 1989; Sabeur et al., 1993). Despite these dif- a pattern of invasive choroid papillae that is ferences, monophyly ofbats was more or less not found in any other vertebrate (Kolmer, assumed between the time Chiroptera was 1910, 1911, 1926; Fritsch, 1911; Duke-En- named by Blumenbach (1779) and the early dler, 1958; Pedler and Tilley, 1969; Buttery 1970s, when doubts were first raised con- et al., 1990). cerning the evolutionary origins of bats A number ofwell-preserved Eocene fossils (Gregory, 1910; Simpson, 1945; Jones and provide our earliest record of bat evolution. Genoways, 1970; Smith, 1980). Several taxa (e.g., Icaronycteris, Palaeochi- ropteryx) once considered to be possible an- ORIGINS OF THE BAT MONOPHYLY cestors of all extant bats are now believed to represent early branches of the microchirop- CONTROVERSY teran lineage (Novacek, 1985a, 1987; Ha- Jones and Genoways (1970) were the first bersetzer and Storch, 1987, 1992). Charac- to explicitly suggest that Chiroptera might be ters supporting placement of these taxa in diphyletic. They discussed the differences be- Microchiroptera include features of the ear, tween Megachiroptera and Microchiroptera, basicranium, dentition, and postcranial skel- and pointed out that similarities between eton (Novacek, 1985a, 1987). Although many these taxa principally involve the flight fossils are too fragmentary to assess for most mechanism. This raised the prospect that of these characters, dental morphology sug- "convergent evolution attendant with devel- gests that virtually all Eocene bats currently opment of aerial locomotion"-rather than known belong to Microchiroptera. One ex- shared ancestry-might account for similar- ception is a specimen from the Late Eocene ities between megachiropteran and micro- ofThailand, an isolated tooth which appears chiropteran bats (Jones and Genoways, 1970: to be a lower premolar of a megachiropteran 5). This idea was further discussed by Smith bat (Ducrocq et al., 1993). (1976, 1980), and the first data supporting The best-preserved putative megachirop- bat diphyly were presented by Smith and teran is Archaeopteropus, which is known only Madkour (1980). Subsequent discussions from a single partial skeleton from the Late have focused on relationships of Megachi- Oligocene of Italy (Meschinelli, 1903). The roptera and Microchiroptera to each other skull and dentition ofthis specimen are badly and to other mammalian groups, particularly damaged, but some evidence suggests that various "archontan" mammals including Archaeopteropus might have had an insectiv- Primates, Dermoptera (colugos or gliding le- 4 AMERICAN MUSEUM NOVITATES NO. 3103 murs), Scandentia (tree shrews), and extinct ymous with Pettigrew's hypothesis of rela- Plesiadapidae and Paromomyidae (fossil tionships (i.e., Megachiroptera is more close- forms generally considered related to either ly related to Primates and Dermoptera than primates or dermopterans). With the possible to Microchiroptera). This overlooks the pos- exception ofParomomyidae, all ofthese taxa sibility that Megachiroptera might be related appear to be monophyletic (Zeller, 1986; Wi- to an entirely different set of taxa; Pettigrew ble and Covert, 1987; Kay et al., 1992; Beard, and his colleagues might be correct about bat 1993a). diphyly, yet wrong about the relationships of Smith and Madkour (1980) identified six Megachiroptera and Microchiroptera to oth- derived morphological characters that Mega- er mammals. To avoid confusion between chiroptera shares with archontan taxa other the general concept of bat diphyly and Pet- than Microchiroptera, including features of tigrew's hypothesis of relationships, the the penis, brain, wrist, and dentition. Inad- phrase "bat diphyly sensu Pettigrew et al. equate character descriptions and lack of ev- (1989)" is used in the following discussions idence for homology of some derived char- to specify the phylogenetic hypothesis sup- acter states compromised the results of their ported by Pettigrew and his colleagues. phylogenetic analysis (see discussion under Results of Morphological Studies), and few REVIEW OF PHYLOGENETIC systematists accepted Smith and Madkour's STUDIES (1980) conclusion that bats are diphyletic. Hill and Smith (1984) favored the diphyly Many different types of molecular and hypothesis but presented no new data. morphological data have been used in studies In the late 1980s Pettigrew and his col- relevant to the bat monophyly controversy leagues reported a series of derived features (tables 1, 2). Some studies have focused on of the nervous system that support chirop- data from a single protein, gene, or organ teran diphyly. The phylogeny they presented system, while others have attempted to in- suggests that Megachiroptera is more closely tegrate diverse types of data. In general, two related to Primates and Dermoptera than it categories of data may be recognized: dis- is to Microchiroptera, which falls well outside tance data and discrete character data. "Archonta" and may represent one of the Distance data consist of measurements of most basal branches within Eutheria (Petti- continuous variables estimated in a series of grew, 1986, 1991a, 1991b; Pettigrew and pairwise comparisons. The "evolutionary Cooper, 1986; Pettigrew and Jamieson, 1987; distance" separating taxa is calculated at the Pettigrew et al., 1989). Over 20 derived neu- end of a study by combining data from the ral traits and one postcranial character have comparisons to form a consensus hypothesis. been cited as supporting this hypothesis, al- Distance techniques (e.g., immunodiffusion, though some of these features have yet to be DNA-DNA hybridization) offer methods for studied in all of the relevant taxa (see sum- estimating relationships among taxa, but un- mary in Pettigrew, 1991 a). Methods of phy- fortunately provide few means of evaluating logenetic analysis and details ofseveral char- the nature ofthe evidence supporting various acters employed by Pettigrew and his relationships. Goodness-of-fit statistics may colleagues have been questioned by various be employed to evaluate trees, and replica- authors (e.g., Wible and Novacek, 1988; Ba- tions may be performed to calculate confi- ker et al., 199 lb; Simmons et al., 1991; Thiele dence limits, but problems exist with under- et al., 1991; Johnson and Kirsch, 1993; Kaas lying assumptions of additivity of distances and Preuss, 1993; Simmons, 1993). How- (Felsenstein, 1984). Distance data do not per- ever, aspects of the neural data are compel- mit formulation or testing of hypotheses of ling, and subsequent debate of Pettigrew's homology, and patterns of transformation conclusions stimulated many morphological cannot be investigated. Subsets of data from and molecular studies (tables 1, 2, 3). different sources cannot be combined, and it In part as a result ofhistorical development is difficult to compare results ofdistance anal- of the controversy, some authors in recent yses with those ofdiscrete character analyses years have treated "bat diphyly" as synon- except to note general agreement or disagree- 1994 SIMMONS: CHIROPTERAN MONOPHYLY 5 ment concerning phylogenetic results (i.e., tree included only one species from each of the topology). Nevertheless, distance techniques bat suborders (e.g., Mindell et al., 1991), while provide a valid means for constructing phy- others have examined multiple species rep- logenies (Felsenstein, 1984; Sarich, 1993), and resenting most or all extant families (e.g., some studies involving distance data are rel- Smith and Madkour, 1980). Sampling ofbats evant to the issue of bat monophyly. in the majority of phylogenetic studies falls In contrast to distance techniques, analyses somewhere between these extremes (tables 1, ofdiscrete character data (e.g., morphological 2). Taxonomic sampling of other mamma- traits, amino acid sequences, nucleotide se- lian orders has similarly varied. Represen- quences) require formulation and testing of tatives of each of the non-bat archontan or- explicit hypotheses of homology. Subsets of ders (Primates, Dermoptera, and Scandentia) data from different sources (e.g., anatomical are represented in most recent studies be- systems) can be combined in comprehensive cause these taxa are central to the bat mono- analyses or analyzed separately depending on phyly controversy. However, sampling with- the goals of the study. When phylogenetic in these groups has been uneven, and other analyses have been completed, both tree to- orders of mammals considered crucial by pology and the evidence supporting various some authors (e.g., Insectivora, Carnivora) clades (i.e., synapomorphies) can be exam- have been omitted entirely from many phy- ined, and results of different studies can be logenetic analyses (tables 1, 2). Studies rele- compared. Levels ofhomoplasy in characters vant to bat monophyly range from those in- supporting a given clade can be considered cluding representatives of only three when evaluating the strength of the overall mammalian orders (e.g., Mindell et al., 1991) evidence supporting a particular phylogenet- to those including representatives ofall ofthe ic conclusion. However, analyses of discrete extant orders (e.g., Sarich, 1993). character data are subject to their own set of Taxonomic sampling is often effectively problems, including character dependence constrained by the type of data under con- and problems associated with various sideration. Among molecular studies, the time weighting schemes. All such issues must be and expense involved in nucleotide sequenc- considered when evaluating the results of ing have apparently discouraged workers from phylogenetic studies (see discussion in Sim- attempting to sample broadly (table 1), al- mons, 1993). though this is now changing with the increased use of PCR and universal primers. Studies involving amino acid sequence data TAXONOMIC SAMPLING tend to include a much broader sample of One methodological issue ofprime impor- taxa because comparable data for many taxa tance in the bat monophyly controversy is have been collected over the years in con- taxonomic sampling (Baker et al., 199 lb; junction with different projects (table 1; Cze- Simmons, 1993). Both chiropteran suborders lusniak et al., 1990). Among morphological present problems because of their enormous studies, types of characters that can be ob- diversity. Megachiroptera comprises over 150 served only with intensive, laboratory work extant species referred to a single family, and (e.g., neural characters, fetal membranes) are Microchiroptera includes over 750 extant generally surveyed in fewer taxa than data species referred to 16 families (Koopman, which can be easily obtained from standard 1993). Because these taxa are speciose, stud- museum preparations (e.g., craniodental ies of higher-level relationships must settle characters). Fossil taxa potentially relevant for sampling only a subset of the species in- to the question ofbat monophyly (e.g., Icar- cluded in each group. This is also true for onycteris, paromomyids) can be considered other relevant taxa including Primates (233 only in the context ofmorphological data sets species) and Scandentia (19 species; Groves, that include characters preserved in fossils 1993; Wilson, 1993). (e.g., craniodental characters, vascular fea- Not surprisingly, taxonomic sampling has tures associated with osteological features). been highly uneven in studies relevant to bat Breadth and intensity of taxonomic sam- monophyly (tables 1, 2). Some studies have pling can affect the results of phylogenetic 6 AMERICAN MUSEUM NOVITATES NO. 3103 studies in several ways, influencing both to- ble 1). Results of more comprehensive im- pology oftrees and perceived support for var- munodiffusion experiments involving addi- ious relationships (Gauthier et al., 1988; tional mammalian orders have never been Donoghue et al., 1989; Novacek, 1992b, fully reported, but Sarich (1993: 105) stated 1994; Simmons, 1993). In studies relevant to that results of such experiments "unequivo- bat monophyly, taxonomic sampling does not cally support bat monophyly." appear to have had much impact on one cen- Kilpatrick and Nunez (1993) and Nunez tral phylogenetic conclusion-virtually all of and Kilpatrick (in press) have reported in ab- these studies support monophyly of bats (ta- stracts the results of a DNA-DNA hybrid- bles 1, 2). However, different studies have ization study that included bats and members reached different conclusions concerning re- of three other mammalian orders (table 1). lationships of Chiroptera to other mamma- Results of bootstrap analyses indicate some lian orders, results which appear to be due at ambiguity in the data (Kilpatrick and Nunez, least in part to sampling effects (see Discus- 1993), but phylogenetic trees generated from sion and Conclusions below). The perceived analysis of mean estimates of genetic diver- support for bat monophyly (or any other clade gence and normalized percent of hybridiza- identified in a phylogenetic analysis) depends tion were interpreted as supporting mono- upon the specific taxa considered and the rel- phyly of Chiroptera (Kilpatrick and Nunez, ative "phylogenetic distance" between the 1993; Nunez and Kilpatrick, in press). groups included in the study. Poor sampling within bats may falsely indicate that some AMINO ACID SEQUENCES variable characters are fixed synapomorphies of Chiroptera, or may suggest that characters Pettigrew et al. (1989) were the first to use are ambiguous when they in fact are not. Poor amino acid sequence data to address rela- sampling of other mammalian orders may tionships of Megachiroptera and Microchi- have similar effects, and support for chirop- roptera. A series of "preliminary" phyloge- teran monophyly may be over- or underes- netic trees produced from analyses off-globin timated if the true sister group ofbats (what- amino acid sequences in bats and members ever taxon that may be) is absent from a study. of seven other mammalian orders were in- These possibilities indicate that sampling terpreted by Pettigrew et al. (1989) as sup- methods must be considered when inter- porting bat diphyly. However, Baker et al. preting results of phylogenetic analyses. (1991b) disagreed with that interpretation, pointing out that diphyly of Microchiroptera RESULTS OF BIOCHEMICAL AND and Primates-rather than Chiroptera-was MOLECULAR STUDIES indicated by topology of the f-globin trees. A wide variety of biochemical and molec- Pettigrew (1991 a) added several taxa (and apparently some a-globin sequences) to the data ular data have been used in to re- attempts set, and upon reanalysis concluded that the solve bat relationships (table 1). Some studies hemoglobin data are ambiguous concerning have produced inconclusive results, but the bat majority support relationships. monophyly of Chiroptera. The hemoglobin studies discussed by Pet- In no case have molecular data provided un- tigrew and his colleagues are difficult to in- ambiguous support for bat diphyly. terpret because the data have never been published, and it is not entirely clear which globin IMMUNOLOGICAL DISTANCE DATA AND sequences were considered by Pettigrew DNA-DNA HYBRIDIZATION (199 la). In other studies, Stanhope et al. The use of immunological data in studies (1993) reported that analyses including both ofhigher-level relationships ofmammals was a-globin and 3-globin amino acid sequences reviewed recently by Sarich (1993). Cronin provide support for bat monophyly. Stan- and Sarich (1980) reported that albumin im- hope et al. (1993) argued that Pettigrew munological distance data from bats and (1991 a) had used exactly the same a-globin members of four other mammalian orders and f-globin data employed in their studies, provide clear support for bat monophyly (ta- but that his analytical procedures had not 1994 SIMMONS: CHIROPTERAN MONOPHYLY 7 allowed him to identify the most parsimo- Jong et al. (1993: 9) concluded that the aA- nious tree for the subset of taxa analyzed. crystallin sequence data were "indecisive as Stanhope et al.'s (1993) reanalysis ofthis data to the mono- or biphyletic origin of Micro- subset (a- and ,B-globin from 52 mammal spe- and Megachiroptera." cies) indicated monophyly of Chiroptera, although support for this grouping was weak. rDNA RESTRICTION SITES In trees only one step longer than the shortest Baker et al. tree, two clades of bats (one ves- (199 la) mapped 52 rDNA re- containing striction sites in bats and members of four pertilionids and another containing the remaining megachiropterans and microchirop- other mammalian orders (table 1). A total of 28 variable sites were identified, including 17 terans) apparently occur as separate branches that were potentially at an unresolved node, thus suggesting that phylogenetically infor- both Chiroptera and Microchiroptera might mative (Baker et al., 1991 a). Unfortunately, relationships of Megachiroptera and Micro- be paraphyletic. Bat monophyly sensu Pet- chiroptera could not be resolved this tigrew et al. (1989) was not supported in any using data set. A tree consistent with bat of the near most parsimonious trees exam- diphyly ined by Stanhope et al. (1993). sensu Pettigrew et al. (1989) was found to be one step shorter than the bat monophyly tree Analyses of more comprehensive amino presented by Wible and Novacek (1988), but acid sequence data sets data from (including this difference was interpreted as insignificant a- and aA crys- f-globins, myoglobins, lens (Baker et al., 199 la, 199 lb). Parsimony anal- tallins, fibrinopeptides, cytochrome c, ribo- ysis resulted in discovery of numerous trees nucleases, and embryonic a- and 3-globins) also weak two steps shorter than the "bat diphyly" tree, provide support for bat monophyly and a strict consensus of these (Czelusniak et al., 1990; Stanhope et al., produced a 1993). A phylogenetic tree poorly resolved tree which indicated non- published by Cze- monophyly ofPrimates and Microchiroptera lusniak et al. (1990: fig. 3) indicated paraphyly of Chiroptera, but in text as well as Chiroptera (Baker et al., 1991 a). the (p. 565) Pettigrew's (1991a) claims to the contrary, the authors noted that addition of a- and the rDNA restriction site data presented to 3-globin data from another microchiropteran date do not appear to provide a useful guide (Tadarida) changes the tree topology so that Chiroptera is monophyletic. The evidence to higher-level relationships among archon- placing bats together within this tree must tan mammals. have come a- principally from and f-globin DNA SEQUENCES data, as these were the only proteins sampled in multiple bat species (Czelusniak et al., Although most studies of DNA sequences 1 990). have included comparatively small numbers de Jong et al. (1993) reported results of a of taxa (table 1), these studies have generally study of aA-crystallin amino acid sequences produced conclusive results. Strong support from bats and members of 17 other mam- for bat monophyly has come from nucleotide malian orders (table 1). Among the mammals sequence analyses of two nuclear genes, the considered, sequence variation in the aA- E-globin gene (Bailey et al., 1992) and the gene crystallin chain occurs at 62 positions (de Jong for interphotoreceptor retinoid binding pro- et al., 1993: table 2.1), and substitutions at tein (Stanhope et al., 1992, 1993). Chirop- 32 ofthese positions may be phylogenetically teran monophyly has also been supported by informative. Parsimony analysis of this data analyses of nucleotide sequence data from set suggests bat diphyly, but only two addi- two mitochondrial genes, the cytochrome ox- tional steps are required to place bats together idase subunit II gene (Adkins and Honeycutt, in a monophyletic group (de Jong et al., 1993). 1991, 1993), and the 12S rDNA gene (Min- Because data from only three bat species dell et al., 1991; Ammerman and Hillis, 1992; (Pteropus vampyrus, P. scapulatus, and Ar- Knight and Mindell, 1993; Springer and tibeusljamaicensis) were included in the study, Kirsch, 1993). and only a single unambiguous sequence Bailey et al. (1992) considered the nuclear transformation supported bat diphyly, de E-globin gene (the 5'-most member of the 0 0 0~~~~~

CU .CU 0d

0 Go

0 C t2 _~Cf d > 4 JD C 0 CU (ACU

c E C 0 K 0 o 2~" 3 o LI o0 0 CU CUd

- a.) bo.) o"0 a 0 a.)q Cs 02~C

n -CU~~ ~ ~ ~ ~ ~~(UuiCU U

0+CdC's E C0"0a.)" 00 CUt a.)CU('

C"0&'2z 09 "0' .~~~~~Cd C.).) 0G q A Ci rcs Ps) CU CU~~~~~~~C CU( U~~~~~( 04 1 *-A Go c o UC U > >CU c Ps CA~~~~~CUCUC10

Z~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~'

en cd en.0enCen C41)~~~ ~ ~ ~ ~ ~ ~ ~ ~ ~

N~ 00

~ ~ Cd d C

C'sC

U~~~~~~~C .)dC13

C)~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~C

00~~~~~~ ~ ~ ~ ~ ~ ~ ~~~~~~~~~~~~0

1I -St - -V c) (U t C) C) 0 401 C).- 01 01 C.)w *> 0 o CU 0 0 C.)> 0 :3 4a 8 0 0 0 o 0 "CU 0 CU"1 c) ECU CUd 0~ m m C.) CdU* CU CU CU a

Si 0 1~~~~~~~~~~ C u Go~~~~~~~ El Cd~ ~~~~U z Cd~UU~~I- m CU CU A'~ -C Go~~~~~~ 0~~C'.

i.C 'd

0;-,~C C - .' rA~ ~ ~ ~

- 4 cn 04 CA 0L *) Uv, F-4 0 '0 C.)- .) CU .C ~ r Q C C) 0~~~~~ _- C U .< a ON o ~7 U ;^a I-4C-

C.) O- 01 enON - 0 ON 1U) - ON a-, .-I I-ICU en 1-4 -4 4 cr cr ON > a- C.) (ON(ON x ON ON~ I.) '0 ON'l 0 1- ON crE C)s I_- _- en, * ON 0 '.40;n e '0 'S4 ON o ,CU CZ0 C) CIS ..CU -30 C1) 0 .0-4c .Q '" t .C eu 04 10 m m 1)< - ~~ ~~~CU 0 ,~~~~~~~CU&<~~~~~~ '4-b 0q.% CU*~C- o '~

CU~ ~ ~ ~~~1!9a)'~~~'o ~~ '0

- '0. CUCU~~~~~~~~~~~~~~~~~~~~~~~~0 C~~~~~~~,U,0 . 0 9 00.~~~~~~~~~~~~~~~~~~~~~CU0~~~~~~~~~~~~~~~~~~~~~ ~ ~~~~~~~~ CU~ ~ ~ ~ ~ ~ ~~~A r ~~CC- ~~~~~~~~( W5

0N0CUC' 0 o~0 H ~~~~~CU~~~~~~~~~~~0~) 0 CU

~~~ OCUCU~~~~cc W 0CU,0~~~~~~~~,02

co cis _0 0 L o. ONU0CCC U oN LL~~~~~~~CU U) CU,CU~~~~~~~~o~~~~~~~~~~~~~~~~~~'~~~~C0'~~~~2'0-'0-0 U)0 ~~~~~~~~~~~~~~~~iso 00~ ~ ~ 2 Z-,U

'0 00).~o 0 0 a 4 2 4))CCC~ -. o~ U)00, 2~ CU 0 C cisC-)I ~ I~UUC-~0~ ~ OC

1-4 CU r. C QCU UUO-)C._'0 (U Oa 0O )U ' CUUU~ U ."t onUOCU'00~~U..C~g~~ ', ~ ~ I Gnc

0~~,CU~~~C'0'0CU~~~~C-),CU U) ~~~~~~ ~~'0 O>)U '0 ~C) CU ,CU44-,CU-U)U)~~~~~ '0 ' 0 = a CU. CUC -~ O N U)o U U . U, M CU-4C'0 ;..isO ZC- 0 ~ ~~~~~~ > C-~~~~~~~~~~~CUO~~ 'U) c CU o C ~~'~~~~~C'U)HCUCUH0~~~~~~~~~~~cUd CC's >.CU 1 994 SIMMONS: CHIROPTERAN MONOPHYLY I1I

f-globin gene cluster) to be appropriate for unique in the data set) were identified as syn- investigating bat relationships because this apomorphies of Chiroptera (Stanhope et al., gene appears to have been less prone to tan- 1992, 1993). dem duplications than other d-type globin Adkins and Honeycutt (1991, 1993) com- genes, and because most of the E-globin se- pared nucleotide sequences of 684 base pairs quence is noncoding and thus presumably not of the mitochondrial cytochrome oxidase subject to functional constraints. Over 1200 subunit II gene (COII). The 1991 study in- nucleotide positions of the e-globin sequence cluded two bat species and members of six were sampled in bats and members of five other mammalian orders; the 1993 version other mammalian orders (table 1; Bailey et included four bats and members ofseven oth- al., 1992). Analysis of this data set resulted er orders (table 1). Analyses ofthe COII data in identification of a single most parsimo- with transversions and transitions weighted nious tree which supported monophyly of equally suggested chiropteran paraphyly in Chiroptera (Bailey et al., 1992; Stanhope et both iterations ofthe study. In the 1991 anal- al., 1993). Trees indicating bat diphyly sensu ysis, a rodent nested within the smallest clade Pettigrew et al. (1989) were found to require containing both bats in the most parsimo- over 100 additional evolutionary steps (nu- nious trees (Adkins and Honeycutt, 1991: fig. cleotide substitutions) than the shortest tree 1A). In contrast, bats, primates, and artio- (Bailey et al., 1992). Megachiroptera and Mi- dactyls formed a clade in four equally par- crochiroptera uniquely share 39 derived sub- simonious trees discovered in the 1993 study; stitutions in the E-globin sequence, including monophyly ofArtiodactyla and Primates was 26 substitutions that exhibit no homoplasy supported in all four of these trees, but Pri- in the context of the data set (Bailey et al., mates nested within the smallest clade con- 1992; Stanhope et al., 1993). In contrast, only taining all four bats (Adkins and Honeycutt, two substitutions potentially support a mega- 1993: fig. 3). Microchiroptera appeared as a chiropteran-primate clade or a megachirop- paraphyletic group in all equally parsimoni- teran-dermopteran clade. ous trees, with Rhinolophus appearing as the The gene for interphotoreceptor retinoid sister taxon ofPrimates rather than grouping binding protein (IRBP) is a single-copy nu- with the other microchiropterans (Adkins and clear gene (Stanhope et al., 1992, 1993). Stan- Honeycutt, 1993). However, different results hope et al. (1992) argued that functionally were obtained when an alternative weighting constrained coding DNA sequences such as system was employed. IRBP may be particularly useful for resolving In both interations of Adkins and Honey- ancient phylogenetic branching patterns be- cutt's study, the most parsimonious trees cause the relatively low sequence divergence based on transversions-only data contained seen in such genes facilitates alignment of a monophyletic Chiroptera. Ten nucleotide sequences from divergent mammalian or- substitutions supported Chiroptera in the ders. IRBP sequences ofapproximately 1200 1991 study, while seven substitutions sup- base pairs were collected from bats and mem- ported this group in the 1993 version (Adkins bers of eight other mammalian orders (table and Honeycutt, 1991, 1993). In the 1993 1; Stanhope et al., 1992). Analyses of these study, which included three microchiropter- data were conducted under a series of differ- ans, the topology reconstructed using the ent assumptions (neighbor-joining and par- transversions-only data is consistent with simony, rooted and unrooted trees, marsu- current hypotheses ofmicrochiropteran phy- pials present or absent in data set), and all logeny (e.g., Van Valen, 1979; Luckett, 1980b; results strongly supported bat monophyly Smith, 1980; Pierson, 1986). Microchirop- (Stanhope et al., 1992). In an unrooted par- tera forms a monophyletic group, and Mac- simony analysis of the eutherian taxa, the rotus and Phyllostomus (members of the shortest tree indicating bat diphyly sensu Pet- monophyletic family Phyllostomidae) to- tigrew et al. (1989) required 46 more nucle- gether form a well-supported clade within otide substitutions than the most parsimo- Microchiroptera (Adkins and Honeycutt, nious trees (Stanhope et al., 1992). A total of 1993: fig. 3). 22 nucleotide substitutions (7 of which were Studies of mitochondrial genes frequently 12 AMERICAN MUSEUM NOVITATES NO. 3103 employ transversion weighting, which is gen- (COI; 236 base pairs) in two bats and mem- erally justified based on the expectation that bers oftwo other mammalian orders. Prelim- mitochondrial DNA transition/transversion inary analyses in which transitions and trans- ratios decrease and transition substitutions versions were weighted equally indicated that approach saturation as evolutionary diver- bats were not monophyletic. However, when gence increases (Adkins and Honeycutt, 1991; only transversions were considered, Mindell Mindell et al., 1991). Because the divergence et al. (1991) found clear support for bat times for bats and their possible relatives are monophyly even when the outgroup was var- quite long (55-70 million years; Benton, ied, alternative alignment strategies were em- 1990), transversion weighting has beenjudged ployed, and a gap-coding scheme was used. to be appropriate by most molecular system- When the two data subsets were considered atists testing bat monophyly with mitochon- separately, the 12S data strongly supported drial DNA data (e.g., Adkins and Honeycutt, bat monophyly, but the COI data were am- 1991, 1993; Mindell et al., 1991; Ammerman biguous. Knight and Mindell (1993) exam- and Hillis, 1992; Knight and Mindell, 1993; ined the 12S data for substitution biases, and Springer and Kirsch, 1993). found that transversions involving G (gua- The technique most commonly used to ef- nine) were relatively rare and occurred far fect transversion weighting is simple omis- below expected levels. Suggesting that these sion oftransitions from the analysis (e.g., Ad- rare substitutions may be particularly useful kins and Honeycutt, 1991, 1993; Mindell et for resolving branching patterns of ancient al., 1991; Ammerman and Hillis, 1992). divergences, Knight and Mindell (1993) not- However, questions have been raised reed that two such transversions support bat cently concerning this method (Springer and monophyly, while no substitutions ofthis type Kirsch, 1993; Novacek, 1994; Wheeler, in support a megachiropteran + primate clade. press). Sample size is one area of potential Ammerman and Hillis (1992) also ana- weakness. Springer and Kirsch (1993) point- lyzed mitochondrial 12S rDNA nucleotide ed out that transversion weighting may be sequences. While Mindell et al. (1991) con- problematic when applied to short sequences sidered a relatively large number ofbase pairs, (e.g., .400 base pairs) because of the rela- the taxonomic sampling in that study was tively small number of transversions pre- very poor (table 1). In contrast, Ammerman served in such sequences. Effectively dis- and Hillis (1992) considered a larger sample carding potentially informative data (i.e., oftaxa (four bats and members ofseven other transitions) may be hard to justify in many mammalian orders), but analyzed a shorter cases. sequence of only 257 base pairs (table 1). An Wheeler (in press) and Novacek (1994) ad- unrooted analysis of these data with transi- vocate application of a spectrum of weights tions and transversions weighted equally re- to transversions in order to discover the sulted in two equally parsimonious trees, each threshold values that affect tree topologies. of which supported bat monophyly (Am- Novacek (1994) reanalyzed the COII data merman and Hillis, 1992). Employing sev- from Adkins and Honeycutt's (1991) study eral quantitative measures ofconfidence that and found that bat monophyly was main- can be placed on a hypothesis in the context tained when transversions were given weights ofa particular data set (e.g., g, statistic, boot- either 10 x or 5 x that of transitions, but the strapping, Templeton's test, T-PTP), Am- bat clade collapsed when transversions were merman and Hillis (1992) demonstrated that weighted 2 x transitions. The fact that rela- their phylogenetic results were statistically tively low transversion/transition weighting significant. Additional rooted and unrooted ratios (e.g., 5:1) produce trees in which Chi- analyses including only transversion data also roptera is monophyletic may be interpreted supported bat monophyly (Ammerman and as providing strong support for bat mono- Hillis, 1992). In the unrooted analyses, eight phyly. or nine substitutions (six ofwhich were unique Mindell et al. (1991) analyzed sequence data in the data set) separated bats from the other from mitochondrial 12S rDNA (744 base mammals in the tree (Ammerman and Hillis, pairs) and cytochrome oxidase subunit I genes 1992). 1 994 SIMMONS: CHIROPTERAN MONOPHYLY 13

A third analysis of 12S rDNA data was were included in the study (table 1). Chirop- conducted by Springer and Kirsch (1993). teran monophyly was supported in an un- These authors analyzed a data set of412 base rooted parsimony analysis based on all sub- pairs in two bats and members of 13 other stitutions, and also in an alternative analysis mammalian orders (table 1). While this study including only transversions (Honeycutt and included more taxa and longer nucleotide se- Adkins, 1993). quences than that of Ammerman and Hillis (1992), the goal ofSpringer and Kirsch's study was evaluation of paenungulate relationships, not bat monophyly, and their taxo- RESULTS OF MORPHOLOGICAL STUDIES nomic sampling was limited with respect to Numerous morphological studies have archontan mammals. Members of Dermop- been conducted in recent years, and the ma- tera and Scandentia were not included in the jority of these support bat monophyly (table study, and the bat suborders were each rep- 2). The data employed include features of resented by only a single species (Springer fetal membranes, wing musculature, postcra- and Kirsch, 1993). An analysis of the 12S nial and cranial osteology, vascular system, data including all substitutions (transver- volume of brain components, and combi- sions and transitions) resulted in a mono- nations of these and other data. Only two phyletic Chiroptera in each of four equally data subsets apparently support bat diphyly: parsimonious shortest trees (Springer and features of the nervous system (Pettigrew, Kirsch, 1993: fig. 2). However, some trees 1986, 1991a, 1991b; Pettigrew et al., 1989; only one step longer did not support bat Johnson and Kirsch, 1993) and of the penis monophyly, and a bootstrap analysis could (Smith and Madkour, 1980). The results of not resolve the relationships of bats at a 50 relevant morphological studies of bat rela- percent level (Springer and Kirsch, 1993). tionships are summarized below; putative Another analysis based exclusively on trans- morphological synapomorphies of Chirop- version data failed to support bat monophy- tera are discussed in a subsequent section. ly. Eptesicus (a microchiropteran) grouped Smith and Madkour (1980) investigated with a cetacean in all ten ofthe shortest trees, structure of the penis in bats and members and Macroglossus (a megachiropteran) of five other mammalian orders, and com- grouped with an edentate in nine of the ten bined the penis data with characters from trees (Springer and Kirsch, 1993: fig. 4). Weak other anatomical systems in a phylogenetic support for bat monophyly was found in a analysis. Smith and Madkour (1980) identi- third analysis using Lake's method of invar- fied two derived features of the penis, two iants applied to a data set that included the brain characters, one dental character, and bats, a primate, and a marsupial + mono- one feature of the wrist that Megachiroptera treme group (Springer and Kirsch, 1993). apparently shares with taxa other than Mi- Based on all of their analyses, Springer and crochiroptera (i.e., Dermoptera, Primates, Kirsch (1993: 149) concluded that bat mono- and Scandentia). Lack of similarity of con- phyly received "mixed support" in their ditions lumped together by Smith and Mad- study. While it is clear that bat diphyly sensu kour (1980: 360-361) has resulted in rejec- Pettigrew et al. (1989) was not supported in tion oftwo ofthese putative synapomorphies, any ofSpringer and Kirsch's (1993) analyses, "enlarged neocortex" and "derived, non-in- there also seems to be little clear support for sectivorous dentition" (Wible and Novacek, bat monophyly. Especially given the small 1988; see also Henson, 1970; Campbell, 1980; number ofbat species included in this study, Koopman and Maclntyre, 1980). A third a more appropriate interpretation ofthe data character ("distal radius and lunar carpal and results may be that they are inconclusive broadened") was discussed and rejected by with respct to the issue of bat monophyly. Wible and Novacek (1988) because the dis- Honeycutt and Adkins (1993) combined tribution and potential homologies of these sequences from three genes (COII, IRBP, and modifications were not as indicated by Smith E-globin) in a single, large data set. Bats and and Madkour (1980). The remaining char- members of five other mammalian orders acters-two features ofthe penis and one brain 11

C.)C.) ~ ~ ~ )C ~ U C) U

0 0 0 0 0 0 0 0 Cu0~~~~~~~ ~~~00 0 0 0 0 0 0

co Cu cU uu Cu Cu Cu Cu Cu Cu

Cu ~~~~~~~ 000 Cu Cu ' Cu 0 C 0u C 0 D

o a Cu (Cu1 E 0 Cu C 'dC CuCCua. 0 OCu..-4(Cu) 0 0 U)CuCu cvC.C 0~~~~ ~~~ ,d c Cu (Cu Cu x Cu .)0Cu 0r-'64 U,0 Cu

..., -14 ,. - w 44C Cu~~~~~~~~~~~~~C W5 CCC C '

0,* c CuqCO Co4- 1 <0 C', Cu Ucis

U) Cu.C cs 0 C 0 a '0'

(UGMCF u 0 0 03 -00 >% . ~Cu. C)u 0C "It(L) U) U) .5-C SC.) CZ CIS '~~~~CuC5Cu u ~ ~ UwC' u 'C o Cd~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~C 0 ht 5 U) 0 -o'A d Cu C-) Cu C.) ) W CU &U 0 z 0 z zI p.ci4(isp.4 0 --

ON U U

0 +~~~ oN 00 Cu~ ~ ~ ~ ~~d Cu0-U) 0 U,~~~~~~~+4) 111 -'~~~~~~~~~~.C) Cu-4C Cu~~~~~~~C

~~~ON~0 ~ ~ Cu -> -. Cu C.) U C C S o~~~~~~~~~~~~~ ~~~~~ N2a Cu (A C)-% 64 ~ j .Cu C 0 0 0 0 0 - Cu 0 0 0 -9 CI 0 Cu C u C CuNO cl CZ '0 cu Cu. )1 - Cd~ ~ C)C) - C .-- Cu Cn~~~~~~~~~~~~~~~~~~~C C4u C)C (NC C) - C FD Cuu CA Cu0uC ; C 0 r. .. u u;

C,3~~~~~~~~~~~~~~~~~~~~~~~~~~ )' m o~ u'O~0 Cu-0 . 0. C' OCuOaC))0 - Cu0 H Cu CC),dC) ~~~ C)CuCuCu~~~~~~~~~~~~. C) Cu' 4- O.C4-

0 CZ ~C) C0 C) - ( 0a~10 .- (N C) C.)~~~~~~~~>

C13 C 1%) Cu 13 Cu C)C, Cu H ~~~~~~~~~4br = - 0 > 4 0 a E.COCu 0 ~ C-) C) 0 0000m

00~~~~~~~~~~~~~~~~~~~~~~~C -j0 Co- o,, CZ ) C.) C) C) d 4 '0 C)0o0, 4 CZM~~~~~C o 0 0 Cu Cu Cu Cu'

_00 0 C) 16 AMERICAN MUSEUM NOVITATES NO. 3103 character-provide potential support for the brain components in bats and primates. Un- bat diphyly hypothesis. specified methods were used to derive phy- In the late 1980s Pettigrew and his col- logenetic trees from these data, and statistical leagues reported a series of derived features methods were employed to compare these of the nervous system that suggest that bats trees with the monophyletic and diphyletic are diphyletic (Pettigrew, 1986,1991a, 199 lb; models. According to Lapoint and Baron Pettigrew and Cooper, 1986; Pettigrew and (1993: 64), their ... results corroborate the Jamieson, 1987; Pettigrew et al., 1989). Over monophyletic scenario in every situation ... 20 derived neural traits and one postcranial The diphyletic model, on the other hand, was character have thus far been cited by this found to be as likely as a random phylogeny group in support ofbat diphyly (see summary would be." However, these results must be in Pettigrew, 1991 a). Details ofseveral ofthe considered preliminary until a detailed ac- characters employed in this study have been count of this study has been published. questioned by various authors (e.g., Wible Luckett (1977, 1980a, 1980b, 1985, 1993) and Novacek, 1988; Bakeretal., 199 ib; Sim- extensively studied patterns of fetal mem- mons et al., 1991; Thiele et al., 1991; Johnson brane formation in mammals and interpreted and Kirsch, 1993; Kaas and Preuss, 1993; these ontogenetic and morphological data in Simmons, 1993), but it seems clear that neu- a phylogenetic context. To evaluate bat re- ral characters as a group strongly support bat lationships, Luckett (1 980b) developed a diphyly. This conclusion is also supported by character set of features of fetal membranes alternative analyses recently conducted by and the forelimb, surveyed these characters Johnson and Kirsch (1993). in extant archontan mammals (table 2), as- Johnson, Kirsch, and their colleagues are sessed polarity by reference to numerous oth- responsible for a series of influential papers er mammalian orders, and conducted a man- entitled "Phylogeny Through Brain Traits" ual cladistic analysis ofthese data. Results of (Switzer et al., 1980; Johnson et al., 1982a, this study indicate that bats are monophy- 1982b, 1984, in press; Kirsch, 1983; Kirsch letic; putative synapomorphies ofChiroptera and Johnson, 1983; Kirsch et al., 1983). In include four derived features of the forelimb a reanalysis of data described in these pub- and two features of the fetal membranes lications, Johnson and Kirsch (1993) found (Luckett, 1 980b). Luckett (1993) subsequent- that their neural characters (many of which ly conducted a revised analysis which in- differ from those employed by Pettigrew and cluded data from fetal membranes and the his colleagues) support bat diphyly. Addition basicranium in archontans, rodents, and lag- of five characters from Pettigrew's data set omorphs. Results of this new analysis simi- changed topology of the most parsimonious larly supported chiropteran monophyly, and tree somewhat, but diphyly of bats was still three uniquely derived features offetal mem- supported when only neural characters where branes were interpreted as synapomorphies considered in the analysis (Johnson and of bats (Luckett, 1993). Kirsch, 1993). However, when neural data Wible and Novacek (1988) described sev- (29 characters) were combined with data from eral new features of the skull and vascular other anatomical systems (65 characters from system ofbats, reviewed the literature on bat Novacek et al., 1988), the results were strik- morphology and phylogeny, and summarized ingly different-bats formed a monophyletic data supporting bat monophyly. Their review group in the most parsimonious tree (John- effectively considered all data relevant to the son and Kirsch, 1993). Specifics of the syn- bat monophyly controversy that had been apomorphies supporting Chiroptera were not published as of 1987 (e.g., Luckett, 1980b; discussed by these authors. Smith and Madkour, 1980; Calford et al., One additional study focusing on brain 1985; Pettigrew, 1986; Pettigrew and Cooper, morphology and bat phylogeny has been re- 1986). A total of 22 derived features supported but details of this work have not yet porting bat monophyly were identified by been published. Lapoint and Baron (1993) Wible and Novacek (1988: table 3), including described in an abstract the results of mor- six cranial characters, nine osteological fea- phometric comparisons of volumes of 12 tures of the postcranium, three muscular 1 994 SIMMONS: CHIROPTERAN MONOPHYLY 17 characters, three features of the fetal mem- cranioskeletal features offossil and living ar- branes, and one neural character. Although chontans, although they did not conduct an the cranial characters were rejected by Pet- explicit parsimony analysis of their data. tigrew et al. (1989: table 8), criticisms leveled Based on various morphological compari- at these characters did not adequately address sons, Szalay and Lucas (1993) concluded that issues of homology and the possibility of re- Chiroptera is monophyletic, and noted sev- versals within higher taxa (Baker et al., 199 ib; eral cranial and postcranial synapomorphies Wible and Martin, 1993). Baker et al. (199 lb) of bats. published a tabular summary of the putative Wible and Martin (1993) examined the de- bat synapomorphies reviewed by Wible and velopment of the tympanic roof and floor in Novacek (1988) and added five postcranial a variety of archontan mammals, and devel- features to the list. However, these additional oped a character set based on results of their characters were not discussed further by Ba- study (table 2). Although no explicit parsi- ker et al. (199 lb) and they have never been mony analysis was conducted, they identified properly described or evaluated. two derived basicranial features that are Thewissen and Babcock (1991, 1993) in- unique to bats, confirming some ofthe results vestigated morphology and innervation ofthe published earlier by Wible and Novacek propatagial muscle complex ofbats and other (1988). volant mammals (table 2). Wible and No- Kay et al. (1992) conducted a cladistic vacek (1988) had listed "occipitopollicalis analysis of archontan mammals in order to muscle present on leading edge of propata- assess the affinities of the extinct paromo- gium" as a synapomorphy of bats, but Pet- myid Ignacius (table 2). For this purpose they tigrew et al. (1989) rejected this character on developed a set of33 cranial characters which the grounds that other volant mammals have could be scored in both extant and extinct propatagial muscles as well. In 1991 Thewis- groups. The fossil form Asioryctes, a putative sen and Babcock identified a uniquely de- primitive eutherian, was included as an out- rived pattern of innervation in the propata- group to polarize characters (Kay et al., 1992). gial muscle ofbats (m. occipitopollicalis) that A heuristic parsimony analysis of the com- suggests that presence ofthis muscle is indeed plete data set resulted in discovery ofa mono- a synapomorphy of Chiroptera. Expanding phyletic Chiroptera (Kay et al., 1992). A sec- their study to include additional taxa and ond abbreviated data set was compiled by other features of the propatagium (table 2), assuming monophyly of Megachiroptera, Thewissen and Babcock (1993) confirmed the Microchiroptera, Primates, and Erinaceo- uniquely shared pattern of muscle innerva- morpha, and scoring each with the hypo- tion, and went on to identify two additional thetical ancestral character states implied by features that indicate a single evolutionary the initial heuristic analysis. Not surprisingly, origin for the propatagial muscle in bats. monophyly of bats was supported by ex- These data were interpreted as supporting haustive search analyses of this second data monophyly of Chiroptera (Thewissen and set, and two unique cranial synapomorphies Babcock, 1991, 1993). of Chiroptera were identified. The shortest In order to evaluate the phylogenetic re- "bat diphyly" tree sensu Pettigrew et al. (1989) lationships ofa variety ofextinct archontans, was found to be seven steps (17%) longer than Beard (1993a) developed a data set of post- the most parsimonious tree (Kay et al., 1992). cranial, cranial, and dental characters which Simmons (1993) summarized previously he surveyed in both extant and extinct forms published morphological character data from (table 2). An exhaustive parsimony analysis most of the studies described above,2 and of these data resulted in discovery ofa single conducted a cladistic analysis of this inte- most parsimonious tree in which Chiroptera grated data set (table 2). A total of 154 char- is monophyletic (Beard, 1993a). One unique acters in 6 subsets were included in Simmons' cranial and six postcranial characters were identified as synapomorphies ofbats (Beard, 2 Exceptions are a number of characters described for 1993a). the first time in Baker et al. (199 ib), Kay et al. (1992), Szalay and Lucas (1993) also examined and Wible and Martin (1993). 18 AMERICAN MUSEUM NOVITATES NO. 3103

(1993) study: cranial features excluding au- eycutt, 1991). A total of 49 morphological ditory region (33 characters), auditory region characters plus variable sites from 684 base (20 characters), anterior axial skeleton and pairs of nucleotide sequence were included forelimb (31 characters), hindlimb (35 char- in the data set (Novacek, 1994). Unweighted acters), reproductive tract and fetal mem- parsimony analysis of the entire data set (in- branes (12 characters), and nervous system cluding both transitions and transversions) (23 characters). These characters were scored resulted in two equally parsimonious trees, in seven extant taxa (Megachiroptera, Micro- each of which supports monophyly of Chi- chiroptera, Galeopithecidae, Strepsirhini, roptera. A second analysis involving trans- Tarsiiformes, Anthropoidea, Scandentia) and versions plus morphological characters (tran- three extinct taxa (Plesiadapidae, Par- sitions omitted) produced a single most omomyidae, Micromomyidae); polarities parsimonious tree that similarly supports bat suggested by the original author(s) of the monophyly (Novacek, 1994). characters were accepted for the purposes of the study. The data thus collected were an- SUMMARY alyzed under a variety of different assumptions, including different weighting systems, The molecular and morphological studies different approaches to taxonomic polymor- summarized above provide strong support phism, inclusion and exclusion offossils, etc. for chiropteran monophyly (tables 1, 2, 3). Support for bat monophyly was found in ev- Analyses of some molecular data sets have ery analysis (Simmons, 1993). Although some yielded ambiguous results concerning bat re- data subsets apparently support bat diphyly lationships (e.g., rDNA restriction sites, aA- (neural data), paraphyly (reproductive tract crystallin amino acid sequences, COI gene + fetal membranes), or are ambiguous (au- sequences). However, analyses of most bio- ditory characters), the combined data set chemical and molecular data support mono- clearly supports bat monophyly (Simmons, phyly of Chiroptera (e.g., albumin immu- 1993). Simmons warned that the results of nological distances, a-globin + f-globin this analysis should be considered prelimi- amino acid sequences, nuclear E-globin and nary because problems were detected with IRBP gene sequences, mitochondrial 12S the coding schemes and polarization criteria rRNA and COII gene sequences). In no in- applied to certain characters. However, sub- stance have molecular data provided un- sequent analyses of a corrected data set in- ambiguous support for bat diphyly. cluding representatives of all of the mam- Morphological data show a slightly differ- malian orders have yielded the same ent pattern (table 2). Neural and penial char- phylogenetic results (Simmons, in prep.). The acters generally support diphyly of bats, but shortest "bat diphyly" trees are more than other data subsets clearly support bat mono- 20 steps longer than the most parsimonious phyly (e.g., characters of the cranium and trees, all ofwhich indicate monophyly ofChi- postcranial skeleton, vascular system, mus- roptera (Simmons, in prep.). cles, and fetal membranes). Studies combining morphological data from many anatom- RESULTS OF STUDIES COMBINING ical systems strongly support bat monophyly even when characters of the penis and ner- MORPHOLOGICAL AND MOLECULAR DATA vous system are included in the analysis Only one study completed thus far has in- (Johnson and Kirsch, 1993; Simmons, 1993, cluded both morphological and molecular in prep.; Novacek, 1994). Chiropteran mono- data in single parsimony analysis (table 3). phyly is also supported when COII sequence Novacek (1994) combined morphological data and morphological characters are com- data from previous studies (e.g., Luckett, bined in a single analysis (Novacek, 1994). 1980b; Novacek and Wyss, 1986; Novacek, The most parsimonious interpretation of 1986, 1990, 1992a; Wible and Novacek, the diverse morphological and molecular data 1988; Pettigrew et al., 1989; Thewissen and now available is that bats are monophyletic. Babcock, 1991) with nucleotide sequence data In this context, characters supporting bat di- from the COII gene (from Adkins and Hon- phyly should be interpreted as homoplastic. 1 994 SIMMONS: CHIROPTERAN MONOPHYLY 19

TABLE 3 Analyses Combining Morphological and Molecular Data Study Data Taxa Conclusions Novacek (1994) Diverse morphological Microchiroptera, Megachiroptera, Der- Bats monophyletic data + all substitutions moptera, Strepsirhini, Anthropoidea, in COII gene nucleotide Artiodactyla, Rodentia, and sequencesa Edentata Diverse morphological Same as above Bats monophyletic data + transversions in COII sequences a Data set included 49 morphological characters and information from 684 base pairs of the COII gene (see text for data sources). The morphological data included 14 cranial characters, 22 postcranial characters, 3 characters of the penis, 3 characters of the fetal membranes, and 7 neural characters.

Derived characters shared by megachirop- Interpretation ofsome characters may vary terans and microchipterans represent poten- depending on the phylogenetic placement of tial synapomorphies of Chiroptera. Chiroptera within Eutheria. All of the features listed below would be considered chiropteran synapomorphies if bats nest within MORPHOLOGICAL CHARACTERS Archonta with Dermoptera as their sister SUPPORTING BAT MONOPHYLY group (sensu Novacek and Wyss, 1986; Wi- As discussed above, a large number of de- ble and Novacek, 1988; Novacek, 1986, 1990, rived morphological characters indicate that 1992a, in press; Johnson and Kirsch, 1993; Chiroptera is a monophyletic taxon. Unfor- Szalay and Lucas, 1993; Simmons, 1993, in tunately, however, no adequate summary of prep.). Some characters, however, may be these features is available. Some putative considered ambiguous or plesiomorphic if synapomorphies have been widely discussed Archonta is not monophyletic and bats be- in the literature, but others have been cited long elsewhere in the mammalian family tree only in tabular summaries or have never been (sensu Adkins and Honeycutt, 1991, 1993; noted in published discussions of bat mono- Stanhope et al., 1992, 1993). These aspects phyly. In this section I describe those mor- of character interpretation are discussed sep- phological features that appear to be syn- arately for each character below. apomorphies of bats, review the taxonomic distribution of each feature, and discuss ev- DENTITION idence for character polarity. Unreferenced Morphology of deciduous dentition. The statements concerning osteological charac- deciduous dentition of eutherian mammals ters are based on my examination of speci- generally consists of incisors, canines, and mens in the collections ofthe AMNH (Amer- premolars, all of which are replaced by sec- ican Museum ofNatural History, New York) ond generation "adult" teeth during ontog- and the USNM (National Museum of Nat- eny. The form of the deciduous dentition is ural History, Smithsonian Institution, Wash- typically similar to the adult dentition. De- ington, D.C.). Following Simmons (1993), ciduous incisors, canines, and anterior pre- character dependence has been hypothesized molars resemble the teeth that will replace a priori only when two or more features of them, and the posterior deciduous premolars possible ontogenetic and/or functional de- resemble adult molars in form. In all known pendence appear to have identical patterns bats, however, the anterior deciduous den- oftaxonomic distribution. In cases where such tition does not resemble the permanent den- features do not have identical distributions, tition. The deciduous incisors, canines, and they may represent independently evolving first premolar are slender, projecting stylets structures and thus are described separately that are markedly recurved (fig. 1; Leche, below. 1875; Friant, 1963; Sige, 1991). Each tooth 20 AMERICAN MUSEUM NOVITATES NO. 3103 has a long pedicle, and may be tipped with (e.g., Rhinopomatidae, Craseonycteridae, as many as three sharp, curved cusps. This Emballonuridae, Nycteridae, Megadermati- pattern of deciduous dental morphology is dae, Natalidae, Thyropteridae, Vespertilion- unique among mammals. idae, and Molossidae). Exceptions include (1) Living bats also differ from other mam- Phyllostomidae, in which the incisive foram- mals in lacking molariform posterior decid- ina are separated by a bar ofbone connected uous premolars. However, some Eocene bats anteriorly with the facial processes ofthe pre- apparently retained molariform deciduous maxillae; (2) some members of Mormoopi- fourth premolars (Sige, 1991). Because these dae, which have incisive foramina separated bats show affinities with living microchirop- anteriorly by a very thin strut that may not terans (Novacek, 1987; Habersetzer and be ossified; (3) Myzopodidae, which have a Storch, 1987, 1992; Sige, 1991), it seems like- median bar of bone that is connected by a ly that primitive microchiropterans-and the pair of very thin bony struts to the facial most recent common ancestor of Megachi- processes of the premaxillae, which do not roptera and Microchiroptera-had molari- meet at the midline; (4) Rhinolophidae, which form posterior deciduous premolars. Ab- have a median bar of bone but lack connec- sence of these structures is derived within tions between this bar and the facial processes Chiroptera and thus is not diagnostic ofbats. ofthe maxillae (facial processes ofpremaxilla absent); (5) some members ofMormoopidae, in which the incisive foramina are apparently SKULL AND CRANIAL VASCULAR SYSTEM reduced to tiny perforations (it is not clear if Palatal process of premaxilla reduced; left these transmit nerves or only blood vessels); and right incisive foramina fused in midsa- and (6) Furipteridae, Mystacinidae, and Noc- gittal plane. The majority of mammals have tilionidae, which lack patent incisive foram- a premaxilla with a well-developed palatal ina. process that is pierced by a pair of incisive Consideration of the presumed relation- foramina on or near the premaxillary-max- ships among microchiropteran families (sen- illary suture (Novacek, 1986; personal obs.). su Van Valen, 1979; Pierson, 1986; Griffiths A bar of bone derived from the premaxilla and Smith, 1991; Griffiths et al., 1992) sug- extends along the midsagittal plane between gests that reduction of the palatal process of the right and left incisive foramina. This pre- the premaxilla and fusion of the incisive fo- sumably represents the primitive condition ramina are primitive for Microchiroptera and for mammals. In contrast, the palatal process Chiroptera. Separation ofthe incisive foram- of the premaxilla is highly modified in most ina is a condition secondarily derived within bats (Dobson, 1875, 1878; Miller, 1907; An- bats, apparently evolving independently in derson, 1912; Koopman, 1984, in press; Wi- phyllostomoids (1 and 2 above), myzopodids ble and Novacek, 1988). (3), and rhinolophids (4). This interpretation In megachiropteran bats the palatal pro- is supported by major differences in mor- cess of the premaxilla is either lacking or is phology of the anterior palate in these three reduced to a small element that supports the groups (Dobson, 1875, 1878; Miller, 1907; incisor dentition but contributes little to the Anderson, 1912; Koopman, 1984, 1994). Re- palate itself (Anderson, 1912; Wible and No- duction and loss of the incisive foramina (5 vacek, 1988). This morphology is associated and 6 above) are other derived conditions with fusion of the right and left incisive fo- that apparently evolved well within Micro- ramina to form a single opening just anterior chiroptera. to the palatal processes of the maxillae (An- Among eutherian mammals, fusion of the derson, 1912; Wible and Novacek, 1988). incisive foramina is a derived condition that The palatal process ofthe premaxilla is also is limited to bats, some hominoid primates reduced in microchiropteran bats, but mor- (Homo, Pongo), and sirenians (Kay et al., phology of the anterior palate is quite vari- 1992; Novacek, 1986; personal obs.). In si- able. In most microchiropteran families renians, the premaxillae are large and the pal- the right and left incisive foramina are atal process is not reduced (Domning, 1978), not separated by a median bar of bone suggesting that fusion of the incisive foram- 1994 SIMMONS: CHIROPTERAN MONOPHYLY 21

dS z 3mm 3mm

3mm

Fig. 1. Close-up views of the deciduous dentition of megachiropteran bats (A, B) and microchiropterans bats (C-F); see text for discussion. A. Pteropus gouldi (Pteropodidae, Pteropodinae; USNM 284137). B. Eonycteris spelaea (Pteropodidae, Macroglossinae; USNM 294809). C. Lasiurus cinereus (Vespertilionidae; USNM 209475). D. Tadarida mexicana (Molossidae; USNM 147786). E. Thyroptera discifera (Thyropteridae; USNM 143784). F. Carollia perspicillata (Phyllostomidae; AMNH 131770). 22 AMERICAN MUSEUM NOVITATES NO. 3103 ina occurred independently in this taxon. rimal (Novacek, 1986; Wible and Novacek, Relative reduction in the size of the fused 1988). This condition, which is seen in all incisive foramina and consideration of the non-bat archontans, is apparently primitive presumed phylogenetic relationships among for Eutheria. In contrast, the jugal of bats is primates (Martin, 1990) similarly suggest that a relatively small bone confined to the middle the condition in Homo and Pongo is not ho- ofthe zygomatic arch, separated from contact mologous with that seen in bats. Accordingly, with the lacrimal by the intervening zygo- the condition seen in bats-fusion of the in- matic process of the maxilla (Wible and No- cisive foramina and concomitant reduction vacek, 1988). Reduction in the extent of the of the palatal process of the premaxilla-is a jugal and loss of a jugal-lacrimal contact is plausible synapomorphy of Chiroptera. seen even in those taxa which have a well- Postpalatine torus absent. The postpala- developed postorbital process (e.g., Ptero- tine torus is a thick, rounded lip which forms pus). the posterior edge ofthe palate. This structure Reduction ofthe jugal is clearly a condition is found in many eutherians including all non- derived within mammals, but it is not limited bat archontans (with the exception ofLoris), to bats. The jugal is reduced (and lacimal insectivorans, and the putative primitive pla- contact lost) in erinaceomorphs, lagomorphs, cental Asioryctes (Kay et al., 1992). In con- and some rodents (e.g., muroids), and the trast, all bats apparently lack a postpalatine jugal is entirely absent in pholidotans and torus (Kay et al., 1992; personal obs.). The soricomorphs (Carleton and Musser, 1984; posterior edge of the palate flares ventrally Novacek, 1986; Wible and Novacek, 1988). in megachiropteran bats of the genus Epom- Based on the presumed phylogenetic rela- ophorus, but the bone is thin and the lip is tionships ofthese taxa (Miyamoto and Good- not rounded (Anderson, 1912: fig. 36; per- man, 1986; Novacek, 1986, 1990, 1992a), it sonal obs.). seems quite likely that the jugal has been in- Novacek (1986: 83) suggested that "torus dependently reduced in bats, lagomorphs, weak or absent" is the primitive condition pholidotans, and within Insectivora (Wible for placental mammals. However, Kay et al. and Novacek, 1988). If bats nest within a (1992) interpreted this character differently. clade characterized by an unreduced jugal As a convention in their analysis, Kay et al. (e.g., Archonta), reduction ofthe jugal would (1992: 488, 496) accepted the condition seen be parsimoniously interpreted as a synapo- in Asioryctes as primitive for all characters morphy of Chiroptera. because this fossil taxon is believed to be Two entotympanic elements in the floor of "close to the ancestry of all later placental the middle-ear cavity: a large caudal element, mammals." Because Asioryctes has a post- and a small rostral element associated with palatine torus, presence of this structure was the internal carotid artery. Rostral and caudal interpreted as the primitive condition by Kay entotympanics are independent cartilages that et al. (1992), and absence ofa torus was con- are found in the tympanic floor and roof of sidered to be relatively derived. IfChiroptera many eutherian mammals (Klaauw, 1922; nests within a clade that is characterized by MacPhee and Novacek, 1993; Wible and presence of a postpalatine torus (e.g., Ar- Martin, 1993). MacPhee and Novacek (1993) chonta), this polarity assessment is probably recently suggested that presence of at least correct with respect to bats, and absence of one such element may be primitive for Euth- a torus would be parsimoniously interpreted eria. Among eutherians, only bats, dermop- as a derived condition diagnosing Chirop- terans, camivorans, macroscelideans, and the tera. The primitive condition for Eutheria as edentate Dasypus have both rostral and cau- a whole remains ambiguous because mar- dal entotympanics (Klaauw, 1922; Reinbach, supials and a variety of other orders lack a 1952; Hunt, 1974; MacPhee, 1981; Wible, postpalatine torus (Novacek, 1986). 1984, 1993; Wible and Martin, 1993). Hy- Jugal reduced and jugolacrimal contact lost. racoids have also been described as having The jugal of most therian mammals is a rel- both elements (Klaauw, 1922; Wible and No- atively large element that forms the antero- vacek, 1988), but Fischer (1989) recently re- ventral rim ofthe orbit and contacts the lac- ported that the caudal element is really a pro- 1 994 SIMMONS: CHIROPTERAN MONOPHYLY 23 cess ofthe petrosal. Ofthose taxa that possess tympani seen in bats is unique among mam- true rostral and caudal entotympanics, the mals and can thus be interpreted as a syna- internal carotid artery runs in proximity to pomorphy of Chiroptera (Wible and Nova- the rostral element only in bats, dermopter- cek, 1988). ans, and carnivorans (Wible, 1993; Wible and King (1991) studied fetal specimens of Martin, 1993). Ofthese forms, only bats and Pteropus and claimed that megachiropterans carnivorans have a large caudal entotympan- do not exhibit the chiropteran tegmen tym- ic that forms in the posterior and postero- pani morphology described by Wible and medial walls ofthe tympanic floor (Wible and Novacek (1988). However, this argument was Novacek, 1988; Wible, 1993; Wible and refuted by Wible (1992), who demonstrated Martin, 1993). that King had incorrectly identified the teg- Bat and carnivorans share a similar pattern men tympani in skull sections (King's "teg- of entotympanic morphology that includes a men tympani" was actually the alisphenoid). large caudal entotympanic and a small rostral All bat species studied to date exhibit the entotympanic that is associated with the in- unique tegmen tympani structure described ternal carotid artery (Wible, 1984; Hunt, above (Wible, 1992). 1974; Wible and Novacek, 1988; Wible and Proximal stapedial artery enters cranial Martin, 1993). Because entotympanics are cavity medial to the tegmen tympani; ramus apparently absent in miacids (Matthew, inferior passes anteriorly dorsal to the tegmen 1909), the putative fossil sister group of Car- tympani. The majority of eutherians exhibit nivora (Wyss and Flynn, 1993), it seems like- a presumably primitive extracranial course ly that this entotympanic pattern evolved infor the ramus inferior of the stapedial artery dependently in bats and carnivorans (Wible (Wible, 1987, 1993; Wible and Novacek, and Novacek, 1988). Ifso, this pattern would 1988). This pattern involves origin ofthe ra- be interpreted as a synapomorphy of bats. mus inferior from the proximal stapedial ar- However, if miacids actually had entotym- tery within the middle ear space, and anterior panics similar to extant carnivorans (a pos- passage of the ramus inferior through the sibility that cannot be ruled out given the middle ear ventral to the tegmen tympani uncertainties of fossil preservation), and if (Wible, 1987, 1993; Wible and Novacek, bats and carnivorans are closely related (a 1988). In contrast, bats, rodents, lagomorphs, possibility suggested by some molecular data), and macroscelideans exhibit an intracranial then the entotympanic pattern described course for this vessel (Wible, 1987, 1992; Wi- above might apply at a higher taxonomic lev- ble and Novacek, 1988). In these taxa the el and would not be considered a synapo- ramus inferior arises from the proximal sta- morphy of bats. pedial artery within the cranial cavity, and Tegmen tympani tapers to an elongate pro- then runs forward dorsal to the tegmen tym- cess that projects into the middle-ear cavity pani (Wible, 1987, 1992; Wible and Nova- medial to the epitympanic recess. The tegmen cek, 1988). The intracranial ramus inferior tympani ofbats is unique in that it is reduced of these taxa appears to be homologous to and tapers to an elongate process that projects the extracranial ramus inferior ofother mam- anteroventrally into the middle-ear cavity mals because both vessels are accompanied (Wible and Novacek, 1988; Wible and Mar- by the lesser petrosal nerve (Wible, 1987, tin, 1993). This condition stands in contrast 1992; Wible and Novacek, 1988). King (1991) to that seen in most other therians, in which indicated that megachiropterans lack the in- the tegmen tympani lacks an elongate pro- tracranial pattern and instead exhibited the jecting process and instead contributes ex- extracranial course ofthe ramus inferior, but tensively to the roof or wall of the epitym- Wible (1992) demonstrated that King was panic recess (Wible and Novacek, 1988; Wible misled by misidentification of the tegmen and Martin, 1993). Dermopterans resemble tympani. Megachiropterans and microchi- bats in reduction ofthe tegmen tympani, but ropterans both exhibit a similar intracranial the dermopteran tegmen tympani tapers to a course for this vessel (Wible and Novacek, short rather than an elongate process (Wible 1988; Wible. 1992). and Martin, 1993). The styliform tegmen Prior to giving rise to the ramus inferior, 24 AMERICAN MUSEUM NOVITATES NO. 3103 the proximal stapedial artery enters the cra- trast to other mammals in which this fossa nial cavity rostral to or through the tegmen is widest at or near its distal end. Baker et al. tympani in rodents, lagomorphs, and mac- (1991b) suggested that reduction of the su- roscelideans (Wible and Novacek, 1988). In praspinous fossa and enlargement of the in- contrast, the proximal stapedial enters the fraspinous fossa may be synapomorphic for cranial cavity medial to the tegmen tympani bats, but changes in fossa area have yet to be in all bats studied thus far (Wible and No- demonstrated using morphometric tech- vacek, 1988; Wible, 1992). This variation in niques. However, the suite of shape modifi- morphology suggests that the intracranial cations described above, including reorien- course of the ramus inferior evolved inde- tationbfthe scapular spine, is unique to bats. pendently in bats and in a clade containing The scapular spine of most mammals is rodents + lagomorphs + macroscelideans relatively deep and corresponds in height to (Novacek, 1986, 1990, 1992a;WibleandNo- the acromion process, with which it is con- vacek, 1988). The unique condition seen in tinuous (fig. 2). As a result oftheir continuity, bats (proximal stapedial artery enters cranial the scapular spine effectively braces the acro- cavity medial to tegmen tympani; ramus in- mion process against forces transmitted ferior has intracranial course) can thus be through the clavicle. Presence ofa deep scap- considered a synapomorphy of Chiroptera. ular spine is presumably primitive for therian mammals. In contrast, the scapular spine of bats is reduced in height compared with the POSTCRANLAL MUSCULOSKELETAL SYSTEM condition described above (fig. 2; Strickler, 1978; personal obs.). Because the scapular Modification of orientation of scapular spine is low, the acromion process appears spine and shape of scapular fossae; reduction to be more strongly arched and less well sup- of height of spine; presence of a well-devel- ported in bats than in other mammals (Baker oped transverse scapular ligament. The ther- et al., 199 lb). However, a well-developed lig- ian scapula is characterized by presence of a amentous sheet known as the "transverse longitudinal scapular spine that separates two scapular ligament" spans the distance be- areas ofmuscle attachment, the supraspinous tween the acromion process and the vertebral and infraspinous fossae. In most taxa the spine border ofthe scapula in bats (Strickler, 1978: originates opposite the midpoint of the gle- 40). This ligament effectively braces the acro- noid fossa, and the axis ofthe scapular spine mion process, apparently performing much lies either directly in line with the axis of the same function as the scapular spine in rotation ofthe head ofhumerus, or it is offset other mammals (Strickler, 1978; Altenbach, only a few degrees (figs. 2, 3). This condition, 1979). This arrangement is apparently unique which is seen in marsupials, insectivorans, to bats. and non-bat archontans, is presumably prim- All ofthe features described above involve itive for eutherian mammals. In contrast, the the scapular spine and are seen only in bats, scapular spine in all bats originates at the so it seems likely that they represent a single posterior edge of the glenoid fossa, and the character complex. This suite of modifica- long axis of the spine is offset 20-300 from tions-reorientation of the scapular spine, the axis ofrotation ofthe humeral head (figs. modification ofthe shape ofthe scapular fos- 2, 3). This condition is apparently unique sa, reduction in height of spine, and presence among mammals. of a well-developed transverse scapular lig- The shift in orientation ofthe scapular spine ament-is an unambiguous synapomorphy in bats is correlated with changes in the shapes of Chiroptera. of fossae and the gross outline of the scapula Reduction of olecranon process and hu- (fig. 3). Compared with that of other mam- meral articular surface on ulna; presence of mals, the supraspinous fossa of bats has a ulnar patella; absence of olecranon fossa on greatly reduced anterior border and an ex- humerus. The elbow joint of bats is unique panded vertebral border. Because the scap- among mammals in that the ulna has a small ular spine is relatively short, the maximum olecranon process with a greatly reduced hu- width of the infraspinous fossa occurs ap- meral articular surface, and the humerus lacks proximately midway along the fossa, in con- an olecranon fossa (Wible and Novacek, 1988; 1994 SIMMONS: CHIROPTERAN MONOPHYLY 25

5mm

Fig. 2. Two views of the right scapula of selected archontan mammals; see text for discussion. The figures on the left provide an axillary view of the scapula with an oblique view of the glenoid fossa; the glenoid fossa directly faces the viewer in the figures on the right. A. Tupaia glis (Scandentia; USNM 396664). B. Lepilemur mustelinus (Primates; AMNH 170557). C. Cynocephalus sp. (Dermoptera; AMNH 14021). D. Dobsonia crenulatum (Megachiroptera; USNM 543180). E. Vampyrum spectrum (Micro- chiroptera; AMNH 261379). 26 AMERICAN MUSEUM NOVITATES NO. 3103

Fig. 3. Dorsal view of the right scapula of selected archontan mammals; see text for discussion. A. Tupaia glis (Scandentia; USNM 396664). B. Lepilemur mustelinus (Primates; AMNH 170557). C. Cynocephalus sp. (Dermoptera; AMNH 14021). D. Dobsonia crenulatum (Megachiroptera; USNM 543180). E. Vampyrum spectrum (Microchiroptera; AMNH 261379).

Szalay and Lucas, 1993; personal obs.). All the posterodistal surface of the humerus in a living bats also apparently possess an "ulnar shallow groove as the elbow is extended (Wal- patella," an ossification in the tendon of m. ton and Walton, 1970; Szalay and Lucas, 1993; triceps that articulates with the humeral troch- personal obs.). The shallow groove for the ul- lea when the elbow is flexed, and rides over nar patella lies in the area occupied by the 1 994 SIMMONS: CHIROPTERAN MONOPHYLY 27

olecranon fossa in other mammals. The ulnar entirely absent only in bats, cetaceans, lago- patella, which is unique among mammals, is morphs, and some rodents (e.g., Dasyprocta). apparently absent in some well-preserved fos- Consideration of the probable phylogenetic sil Eocene microchiropterans (e.g., Icaronyc- relationships of these taxa (Miyamoto and teris; Jepsen, 1966; Szalay and Lucas, 1993). Goodman, 1986; Novacek, 1986, 1990, Despite this observation, the singular mor- 1992a) suggests that absence of a supinator phology of the ulnar patella suggests that this ridge evolved independently in each of these element is homologous in megachiropterans groups. In this context, absence of the supi- and microchiropterans and thus should have nator ridge can be interpreted as a synapo- been present in the common ancestor of bats. morphy of bats. Reduction ofthe olecranon process, reduction Absence of entepicondylar foramen in hu- of the humeral articular surface of the ulna, merus. The entepicondylar foramen (=supra- loss of the olecranon fossa in the humerus, condylar foramen) is a foramen in the distal and perhaps presence of an ulnar patella and humerus that communicates the median patellar groove characterize a unique suite of nerve and brachial artery (Flower, 1885). Al- elbow modifications that is a synapomorphy though presence of this foramen appears to of bats. be primitive for mammals, it is absent in a Extant cetaceans also exhibit reduction of variety of eutherian lineages. For example, the olecranon process and loss of the olec- the entepicondylar foramen is present in most ranon fossa. However, there is little reduction insectivorans but absent in erinaceids, and is in area of the humeroulnar articulation, and present in many carnivorans but absent in reductions in the olecranon process and fossa canids, ursids, and hyaenids (Flower, 1885). are correlated with lateral compression ofthe Among archontan mammals, the entepicon- long bones and development of a transverse dylar foramen is present in dermopterans, ridge on the humerus that restricts movement lemuriformes, tarsiers, and most cebids, but in the anteroposterior plane (Barnes and is absent in other anthropoids and scanden- Mitchell, 1978; personal obs.). Early Tertiary tians (Flower, 1885; personal obs.). The en- archaeocete whales retained a moderately tepicondylar foramen is uniformly absent in large olecranon process, and the elbow joint bats (Wible and Novacek, 1988; personal was apparently capable of anteroposterior obs.). If bats are closely related to dermop- movement (Kellogg, 1936; Barnes and terans and primates, absence of the foramen Mitchell, 1978). In this context, it seems most may represent a synapomorphy of bats (Wi- likely that the elbow modifications seen in ble and Novacek, 1988). However, variabil- cetaceans evolved independently ofthose seen ity of this feature within Eutheria suggests in bats. Morphology of the cetacean elbow that it may not be a particularly useful char- joint bears little resemblance to that seen in acter at higher taxonomic levels. bats, and there is no reason to believe that Occipitopollicalis muscle and cephalic vein bats and whales share any derived, homol- present in leading edge of propatagium. Pro- ogous modifications of the elbow. patagial muscles are present only in gliding Absence ofsupinator ridge on humerus. The or flying mammals. In gliding squirrels and supinator ridge is a thin, prominent ridge that dermopterans, the propatagial complex con- runs up the shaft of the humerus from the sists ofoverlapping sheetlike muscles that ex- lateral epicondyle, providing a wide surface tend from the side of the lower jaw to the oforigin for the supinator muscles ofthe fore- forearm and thumb (Thewissen and Babcock, arm (Flower, 1885). A supinator ridge was 1991, 1993; Gray and Sokoloff, 1992). The present primitively in mammals and has been cephalic vein does not accompany the pro- retained in most noncursorial eutherian lin- patagial muscles into the propatagium in these eages, including non-bat archontans (Flower, taxa (Thewissen and Babcock, 1993). In con- 1885; Wible and Novacek, 1988). In many trast, the propatagial muscle in bats (m. oc- rodents and cursorial mammals the supinator cipitopollicalis) is a long, narrow muscle ridge is poorly developed, but the distal end which originates from the occipital region of of the ridge is still visible at the lateral epi- the skull and inserts on the base ofthe pollex condyle. The supinator ridge is apparently and second metacarpal. Tendinous or mus- 28 AMERICAN MUSEUM NOVITATES NO. 3103 cular slips may also originate on the face and joints, support enlarged interdigital flight in the fascia covering the pectoral muscles, membranes (patagia); digits Ill-V lack claws. and tendinous or elastic regions may inter- The length ofthe digits ofthe hand (including vene between muscle bellies (Mori, 1960; metacarpals and phalanges) are less than or Stickler, 1978; Thewissen and Babcock, 199 1, equal to the length of the forearm in most 1993). The cephalic vein accompanies m. oc- mammals, including all cursorial forms. Each cipitopollicalis into the propatagium in all digit in the hand is typically tipped with a bats studied to date (Thewissen and Babcock, claw or homologous structure (nail or hoof). 1993). The primitive condition for both the manus Layers ofthe sheetlike propatagial muscles and pes of mammals consists of five rela- in dermopterans are served by different tively short, clawed digits with a phalangeal nerves, one receiving innervation from cra- formula of2-3-3-3-3 (Flower, 1885; Carroll, nial nerve VII (CN VII) and the other re- 1988). This pattern is retained in edentates, ceiving innervation from cervical spinal insectivorans, non-bat archontans, and most nerves (Thewissen and Babcock, 1991, 1993). other nonungulate eutherians (Flower, 1885; In contrast, individual muscle bellies in the personal obs.). occipitopollicalis complex receive unusual In contrast to other mammals, digits III- dual innervation from both CN VII and cer- V of bats (and sometimes digit II) are mark- vical spinal nerves in at least two megachi- edly longer than the forearm, a specialization ropterans (Pteropus and Haplonycteris) and that facilitates support ofgreatly enlarged in- two microchiropterans (Myotis and Rhino- terdigital patagia (Wible and Novacek, 1988; poma; Thewissen and Babcock, 1991, 1993). personal obs.). Elongation ofthe digits in bats At least one microchiropteran (Tadarida) is accomplished through elongation of the lacks innervation from the cervical nerves, metacarpals and the proximal two phalanges. but consideration of phylogenetic relation- The distal (third) phalanx on digits II-V is ships of the genera in question suggests that often tiny or absent in chiropterans, although this condition is derived within Microchi- the Eocene bat Icaronycteris has a complete roptera (Thewissen and Babcock, 1991, 1993). phalangeal formula of 2-3-3-3-3 (Novacek, Dual innervation of the propatagial muscle 1987). Claws are always absent on digits III- is apparently primitive for both Megachirop- V of bats, and are frequently absent on digit tera and Microchiroptera. II as well (Jepsen, 1966; Novacek, 1987; Wi- The propatagial muscle in flying squirrels ble and Novacek, 1988). Loss of claws and (Glaucomys) has recently been reported to elongation of the digits of the forelimb, as- receive dual innervation like that ofbats (Gray sociated with presence of large interdigital and Sokoloff, 1992). However, Thewissen and patagia, represent a suite of forelimb modi- Babcock (1993) noted that in flying squirrels fications that is unique to bats among mam- the muscle slips innervated by CN VII are mals. restricted to the face and do not extend into Dermopterans, the only other mammals the propatagium. The dual innervation seen that have interdigital patagia, have claws on in individual muscle bellies of m. occipito- all digits of the manus and do not exhibit pollicalis is a pattern unique to bats (Thewis- marked elongation of the digits (Wible and sen and Babcock, 1993). Dual innervation, Novacek, 1988; personal obs.). In dermop- an occipital origin, and a close association terans the medial (second) phalanges are between m. occipitopollicalis and the ce- elongated relative to the proximal (first) pha- phalic vein suggest that the propatagial mus- langes in digits II-V (Beard, 1990, 1993a), cle complex ofbats is uniquely derived within but this modification falls far short of what mammals (Thewissen and Babcock, 1991, is seen in bats. Even ifpresence ofinterdigital 1993). Presence ofm. occipitopollicalis in the patagia is not a synapomorphy ofbats (which propatagium (accompanied by the cephalic would be the case if Chiroptera and Der- vein) thus represents a synapomorphy ofChi- moptera are sister taxa), the relative propor- roptera. tions of the digits and large size of the inter- Digits II-V offorelimb elongated with com- digital patagia are clearly unique to bats. plex carpometacarpal and intermetacarpal In most mammals, the proximal metacar- 1994 SIMMONS: CHIROPTERAN MONOPHYLY 29 pals articulate with each other and with the bic spine present; absence of m. obturator in- distal carpal elements in such a way as to ternus. The acetabulum in most mammals (in- preclude complex movements of the meta- cluding monotremes and marsupials) is ori- carpals. Carpometacarpal joints are simple, ented so that the axis of rotation of the femur allowing only flexion and extension (Flower, projects ventrolaterally from the hip (fig. 4C). 1885; personal obs.). Strong metacarpal lig- The shaft ofthe femur is markedly offset from aments bind the proximal metacarpals to one the femoral head and neck, which are in line another and hinder mediolateral (adduction/ with the axis ofrotation. The combined effect abduction), rotative, and independent move- assures that the shaft of the femur projects ments of these elements. When present, fac- ventrally and slightly laterally, keeping the knee ets associated with intermetacarpal joints are well below the level ofthe sacrum during most simple and facilitate only limited flexion and normal movements. extension. This apparently represents the In contrast to the typical mammalian pat- primitive condition for mammals. tern, the femur of bats projects laterally and Bats are unique among mammals in having slightly ventrally from the hip joint, and the complex carpometacarpal and intermetacar- knee lies on or above the level of the sacrum pal joints (Vaughan, 1959; personal obs.). (fig. 4A, B). This represents an approximate Each metacarpal has a unique set ofproximal 900 rotation in the orientation of the hind- facets for articulation with various convex limb (Wible and Novacek, 1988). This effect and concave surfaces on the distal carpals, has been produced by a pair of major mod- and metacarpals II-V have extensive com- ifications: reorientation ofthe acetabulum to plex facets for articulation with one another face dorsolaterally rather than ventrolater- (Altenbach, 1979; personal obs.). This suite ally, and reorientation of the shaft of the fe- of carpometacarpal and intermetacarpal ar- mur so that it lies approximately in line with ticulations permits extensive mediolateral the axis of rotation of the hip joint (and the movements of the metacarpals (adduction/ head and neck ofthe femur) rather than being abduction) but prevents anteroposterior markedly offset from this axis. These modi- movements. These modifications apparently fications have been accompanied by other brace the wing against the forces of the air- changes, including a dorsolateral tilting ofthe stream and facilitate control ofthe shape and ischium, flaring of the anterior pubes (asso- camber ofthe interdigital patagia during flight ciated with reorientation of the acetabulum), (Altenbach, 1979). and reduction in the neck of the femur (as- The suite of modifications described sociated with reorientation of the shaft rel- above-elongations ofthe digits, loss ofclaws, ative to the head of the femur). This suite of presence ofinterdigital patagia, and presence modifications is unique among mammals. of a highly derived complex of carpometa- M. obturator internus is a hip muscle which carpal and intermetacarpal articulations-is originates from the inner surface of the ob- unique to bats and therefore represents a syn- turator membrane and the bony rim of the apomorphy of Chiroptera. Cetaceans lack obturator foramen, passes out of the pelvic claws and exhibit elongation of some digits cavity dorsally, and then turns laterad to in- (usually II-III or I-IV), but digit elongation sert on the greaeter trochanter of the femur. is accomplished by addition of extra phalan- This muscle is present in the majority of ges to the digits rather than elongation of the mammals including marsupials, insectivo- metacarpals and proximal phalanges, and rans, and non-bat archontans, but it is absent complex carpometacarpal and intermetacar- in all bats studied to date (Humphry, 1869; pal articulations are lacking. There is no rea- Coues, 1872; MacAlister, 1872; Leche, 1886; son to suspect that any of the forelimb mod- Le Gros Clark, 1924, 1926; Howell and ifications of cetaceans and bats are Straus, 1933; Reed, 1951; Vaughan, 1959, homologous. 1970b). Absence of m. obturator intemus 900 rotation of hindlimbs effected by reori- seems to be functionally related to the pelvic entation of acetabulum and shaft of femur; modifications noted above, as the tilting of neck of femur reduced; ischium tilted dorso- the ischium and flaring of the pubes have laterally; anterior pubes widely flared and pu- apparently reoriented the site oforigin ofthis 30 AMERICAN MUSEUM NOVITATES NO. 3103

face of origin, and then negotiate an acute lateral turn of at least 1300 before inserting on the femur. Modifications of the pelvis as- A sociated with reorientation of the hindlimb may thus have precluded retention of this muscle. M. psoas minor is a pelvic muscle that originates on the lumbar vertebrae and inserts on the anterior ramus of the pelvis. In most mammals, this muscle inserts on a small projection known as the iliopectineal process, which is typically located either on the ilium or at the iliopubic junction (Coues, 1872; Leche, 1886; Le Gros Clark, 1924, 1926; Howell and Straus, 1933; Reed, 1951; personal obs.). In bats, however, the insertion of m. psoas minor has shifted ventrally so that it lies entirely on the pubis, well below 1 cm the level ofthe acetabulum (Humphry, 1869; MacAlister, 1872; Vaughan, 1959, 1970b). The projection on which the muscle inserts has also become elongated to form a structure known as the "pubic spine" (fig. 5; Vaughan, 1959; Szalay and Lucas, 1993). Some other mammals (e.g., desman talpine insectivorans) have an enlarged iliopectineal process, but in no other group does m. psoas minor insert on an elongated process of the pubis. The change in location ofinsertion ofm. psoas minor (and development of a pubic spine) is probably functionally associated with reorientation of the acetabulum and flaring ofthe 1 cm anterior pubes, conditions that are related to the 900 rotation in position ofthe hindlimbs. The morphological features described above-90° rotation ofhindlimbs effected by reorientation of the acetabulum and shaft of the femur, reduction ofthe neck ofthe femur, dorsolateral tilting of the ischium, flaring of the anterior pubes, presence ofa pubic spine, Fig. 4. Posterior view of the right half of the and absence of m. obturator internus -ap- pelvis and articulated femur oftwo bats (A, B) and pear to be functionally related and thus seem a scansorial quadruped (C); see text for discussion. to represent a single character complex. This A. Rousettus amplexicaudatus (Megachiroptera; complex is unique to bats among mammals. USNM 278616). B. Eumops perotis (Microchi- Absence of m. gluteus minimus. This mus- roptera; AMNH 15751). C. Tupaia glis (Scanden- cle originates from the illium and inserts on tia; USNM 396664). the greater trochanter of the femur, which it abducts and rotates. M. gluteus minimus is present in most mammals, including mono- muscle so as to prevent effective function of tremes, marsupials, and non-bat archontans the muscle. If m. obturator internus had been (Coues, 1872; Leche, 1886; Le Gros Clark, retained in bats, the muscle would have to 1924, 1926; Howell and Straus, 1933; Ells- pass dorsomedially almost parallel to the sur- worth, 1974). In contrast, m. gluteus mini- 1 994 SIMMONS: CHIROPTERAN MONOPHYLY 31 mus is absent in insectivorans and bats A (Humphry, 1869; MacAlister, 1872; Reed, 1951; Vaughan, 1959, 1970b). If bats nest within a clade characterized by presence of m. gluteus minimus (e.g., Archonta), absence of this muscle may be interpreted as a synapomorphy of bats. This would not be true if bats are closely related to insectivorans. It should be noted that absence of m. gluteus minimus may well represent another feature functionally linked with the suite of hip modifications described above (i.e., those associated with reorientation ofthe hindlimb). However, this cannot be assumed a priori because absence of m. gluteus minimus, un- like the other features, is not unique to bats. Absence of m. sartorius. This muscle originates from the ilium and/or inguinal ligament and inserts on the medial aspect of the tibia. M. sartorius is present in monotremes, marsupials, and most eutherians, including erinaceid insectivorans and non-bat archontans (Coues, 1872; Leche, 1886; Le Gros Clark, 1924, 1926; Howell and Straus, 1933; Fig. 5. Lateral view of the right side of the Reed, 1951; Ellsworth, 1974). Presence ofthis pelvis of a megachiropteran bat (A) and micro- muscle thus appears to be the primitive con- chiropteran bat (B); see text for discussion. Arrows dition for mammals. indicate the location of the pubic spine, the inser- M. sartorius is absent in bats, macrosce- tion site of the psoas minor muscle. A. Dobsonia lideans, and soricid and talpid insectivorans crenulata (USNM 543180). B. Vampyrum spec- (Humphry, 1869; MacAlister, 1872; Leche, trum (AMNH 261379). 1886; Reed, 1951; Vaughan, 1959, 1970b; Wible and Novacek, 1988). Absence of this muscle in some (but not all) insectivorans suggests that m. sartorius has been lost within mopterans; Coues, 1872; Leche, 1886; Le insectivorans, and it has probably also been Gros Clark, 1924, 1926; Howell and Straus, lost independently in bats and macroscelid- 1933; Reed, 1951; Ellsworth, 1974). In con- eans. Ifbats nest within a clade characterized trast, the vastus in bats consists of a single, by presence of m. sartorius (e.g., Archonta), undifferentiated muscle mass (Humphry, then absence of this muscle would be inter- 1869; MacAlister, 1872; Leche, 1886; Reed, preted as a synapomorphy ofChiroptera. This 1951; Vaughan, 1959, 1970b). This unique might not be true if bats are closely related condition is apparently derived within mam- to macroscelideans or insectivorans. mals. Vastus muscle complex not differentiated. Like other muscular modifications noted The vastus complex comprises a set of mus- above, lack of differentiation of the vastus cles that originate on the proximal femur and muscle complex may be functionally asso- insert into the patella and patellar ligament. ciated with reorientation of the hindlimb. These muscles apparently originate from a However, this cannot be assumed a priori single mass which differentiates into several because the number ofdifferentiated muscles muscles during development. Five distinct in the vastus complex may have been reduced vastus muscles are seen in monotremes; three in other mammalian groups (e.g., marsupials, are found in most eutherians (e.g., insecti- dermopterans) for reasons unrelated to hip vorans, scandentians, primates), and two are reorganization. Interpretation of transfor- present in some taxa (e.g., marsupials, der- mations ofthis character in the basal branch- 32 AMERICAN MUSEUM NOVITATES NO. 3103 es of Mammalia is ambiguous, but it seems ally. As a result, the axis ofthe calcaneal tuber clear that a completely undifferentiated vas- no longer intersects the cuboid facet, but rath- tus is unique to bats. er passes through the anterior surface of the Reorientation of upper ankle joint facets on body of the calcaneum. When the foot is ex- calcaneum and astragalus; trochlea of astrag- tended, the calcaneal tuber does not interfere alus convex, lacks medial and lateral guiding with movement at the upper anklejoint. This ridges; tuber of calcaneum projects in plan- suite ofmodifications is unique to bats among tolateral direction away from ankle and foot; therian mammals. peroneal process absent; sustentacular pro- The peroneal process ofthe calcaneum, un- cess of calcaneum reduced, calcaneoastraga- der which the tendon of m. peroneus longus lar and sustentacular facets on calcaneum and passes, projects laterally from the body ofthe astragalus coalesced; absence of groove on as- calcaneum in most mammals. The primitive tragalus for tendon of m. flexor digitorum fi- therian calcaneum was apparently character- bularis. The upper ankle joint in mammals ized by a prominent peroneal process, but the is formed by a series ofarticulations between process has been reduced or lost in a variety the distal tibia and fibula and the astragalus of lineages including bats, tupaiine scanden- and calcaneum. Primitively, the eutherian tians, and extant euprimates (Szalay, 1977, tibia articules with the astragalus, and the 1982, 1984; Szalay and Decker, 1974; No- fibula articulates with both the astragalus and vacek, 1980; Szalay and Drawhorn, 1980; calcaneum (Szalay, 1977, 1984, 1993; Szalay Wible and Novacek, 1988; Szalay and Lucas, and Decker, 1974; Szalay and Drawhorn, 1993). Because ptilocercine scandentians and 1980; Szalay and Lucas, 1993). The proximal some Paleogene euprimates have a distinct articular surfaces ofthe astragalus collective- peroneal process, Wible and Novacek (1988) ly form an "astragalar trochlea," which is typ- suggested that this structure was lost inde- ically saddle-shaped and bounded by medial pendently in bats, tupaiines, and within eu- and lateral guiding ridges. The tibial and fib- primates. Independent loss in bats seems par- ular facets on the astragalar trochlea and on ticularly likely when reorientation of the the calcaneum lie in planes that are oblique calcaneal tuber is taken into account. The to the distal facets for the cuboid and navic- plantolateral orientation of the chiropteran ular, and the axis of the tuber of the calca- calcaneal tuber is unique, and this arrange- neum (which projects in a posterior direction ment effectively precludes presence of a pe- away from the ankle and foot) passes through roneal process (the normal location for the the cuboid facet (Szalay, 1977, 1984, 1993; mammalian peroneal process is occupied by Szalay and Decker, 1974; Szalay and Draw- the base of the calcaneal tuber in bats). horn, 1980; Szalay and Lucas, 1993; personal The lower ankle joint of mammals com- obs.). This arrangement constrains extension prises the joint between the calcaneum and at the upper ankle joint because the tuber of astragalus. Typically, two distinct points of the calcaneum limits movement ofthe tarsus articulation are involved: a lateral calca- relative to the tibia and fibula. neoastragalar articulation, and a medial sus- Bats have a unique upper ankle joint which tentacular articulation (Szalay and Decker, permits almost full extension ofthe foot. The 1974; Szalay, 1977, 1982; Szalay and Lucas, trochlea of the astragalus lies in a plane par- 1993). The sustentacular facet on the calca- allel to that ofthe navicular facet. The troch- neum is located on the sustentacular process, lear surface is smoothly convex and lacks me- a shelflike medial projection from the body dial and lateral guiding ridges (Wible and ofthe calcaneum; the calcaneoastragalar facet Novacek, 1988; personal obs.). The fibular is located on the body itself. The facets for facet on the calcaneum (when present) has these two articulations are separate in mar- shifted its position to the lateral side of the supials, insectivorans, non-bat archontans, base ofthe calcaneal tuber, and in many forms and the majority oftherian mammals (Szalay the plane of the fibular facet lies parallel to and Decker, 1974; Szalay, 1977, 1982; Szalay that of the cuboid facet. The calcaneal tuber, and Lucas, 1993; personal obs.). This pre- rather than projecting in a posterior direction sumably represents the primitive condition away from the foot, is directed plantolater- for Theria. 1 994 SIMMONS: CHIROPTERAN MONOPHYLY 33

Bats are unique in that the sustentacular of the calcaneoastragalar and sustentacular process has been reduced and the calcaneoas- facets on calcaneum and astragalus, and ab- tragalar and sustentacular facets are contin- sence of groove on astragalus for tendon of uous on the medial side of the body of the m. flexor digitorum fibularis-appear to be calcaneum (Szalay and Lucas, 1993; personal functionally related and thus seem to repre- obs.). Wible and Novacek (1988: table 3) not- sent a single character complex. This com- ed that bats have the "calcaneal-astragalar plex is unique to bats among mammals. facet ofthe calcaneum modified from convex Presence of calcar and depressor ossis styl- process to depression or trough." This apiformes muscle. The calcar, a cartilaginous pears to be a somewhat misleading descrip- and/or osseous element that extends from the tion of the same modification: the "depres- calcaneum to support the trailing edge of the sion" or "trough" is actually formed by uropatagium, is a structure unique to bats. coalescence of the two facets, which lie in M. depressor ossis styliformes, the muscle slightly different planes and form a concave that controls the position of the calcar rela- articular facet when fused. Similarly, Beard tive to the tibia and ankle, is also unique. A (1993a) stated that the sustentacular facet is calcar is absent in one pteropodid (Sphaeri- greatly reduced or absent in bats, an impres- as), Craseonycteris, Rhinopoma, a few phyl- sion that follows from identification of the lostomid species, and several Eocene micro- coalesced facets as the calcaneoastragalar fac- chiropterans (including Icaronycteris), but all et. Reduction of the sustentacular process other bats (including Palaeochiropteryx) have contributes to the impression that the sus- a calcar (Anderson, 1912; Jepsen, 1966; Wal- tentacular facet is absent in bats. ton and Walton, 1970; Smith, 1980; Haber- M. flexor digitorum fibularis (=m. flexor setzer and Storch, 1987). Although m. de- hallucis longus) originates from the postero- pressor ossis styliformes has been studied in distal surface of the fibula and the interos- only a few taxa, it appears similar in mor- seous membrane, passes across the ankle me- phology in both megachiropterans and mi- dial to the calcaneum, and inserts into the crochiropterans (Mori, 1960; Vaughan, 1959, ventral surfaces ofthe distal phalanges (Reed, 1970b; personal obs.). On the basis of pre- 1951; Vaughan, 1959). There is a groove for sumed phylogenetic relationships among the the tendon of this muscle on the posterior genera and families in question (Anderson, surface of the astragalus in the majority of 1912; Van Valen, 1979; Smith, 1980; Pier- mammals, including all non-bat archontans, son, 1986; Novacek, 1987), it seems likely and presence of this groove is presumably that the absence of the calcar and m. depres- primitive for mammals (Beard, 1993a). Re- sor ossis styliformes in some bat taxa is a arrangement of the upper and lower ankle secondarily derived condition. Presence of a joints in bats has apparently resulted in a calcar and m. depressor ossis styliformes can somewhat different location for the tendon therefore be interpreted as a synapomorphy of m. flexor digitorum fibularis. In bats, this of bats. tendon apparently passes over the surface of Shape ofdistal facet on entocuneiform. The the calcaneum medial to the deflected cal- distal facet of the entocuneiform in most caneal tuber (Vaughan, 1970b). Accordingly, mammals is very narrow and includes a strong a groove for the tendon ofm. flexor digitorum plantodistal process that interlocks with a fibularis is not present on the astragalus of groove on the plantar surface of the first bats (Beard, 1993a), a condition that is ap- metatarsal (Beard, 1993a). This presumably parently unique to bats among therians. represents the primitive condition for mam- The morphological features described mals. In primates and dermopterans, the dis- above-reorientation of upper ankle joint tal entocuneiform process is wide and the facets on calcaneum and astragalus, a convex plantodistal process is reduced or absent, a astragalar trochlea lacking medial and lateral condition that is relatively derived (Beard, guiding ridges, projection ofthe tuber of cal- 1993a). In contrast, bats have a proximodis- caneum in a plantolateral direction, absence tally shortened entocuneiform with a flat, tri- of the peroneal process, reduction ofthe sus- angular distal facet (Beard, 1993a), a condi- tentacular process of calcaneum, coalescence tion that is also derived with respect to the 34 AMERICAN MUSEUM NOVITATES NO. 3103 A B of the othr pedal digits (fig. 7; Szalay and Lucas, 1993; personal obs.). This elongation effectively extends the length ofdigit I, which has only two phalanges, and brings the claw in line with those of the other pedal digits (each of which have three phalanges). Elon- gation of the proximal phalanx of digit I is unique to bats among mammals. Th proximal phalanx in digit I is not elongated in three microchiropteran groups (Hip- posiderinae, Thyropteridae, and Myzopodi- dae). This difference is correlated with a reduction ofthe number ofphalanges in digits II-V (Walton and Walton, 1970), another condition that is clearly derived within mammals. On the basis ofpresumed phylogenetic relationships among the various families of bats (Van Valen, 1979; Smith, 1980; Pierson, 1986; Novacek, 1987), it seems likely that the ancestral condition for bats consisted of a phalangeal formula of 2-3-3-3-3 with the proximal phalanx ofdigit I elongated. By this interpretation, secondary reduction of the elongated first phalanx ofdigit I evolved con- currently with reduction of the phalangeal formula to 2-2-2-2-2 in some microchiropteran lineages, thus preserving the ancestral 5mm 5mm arrangement of the claws. Therefore, elon- I Fig. 6. Dorsal view of the foot of a megachi- gation of the proximal phalanx of digit ropteran bat (A) and microchiropteran bat (B) (which is seen in Megachiroptera and prim- showing the relative proportions ofthe phalanges. itively in Microchiroptera) can be interpreted Note that the proximal phalanx of digit I (right as a synapomorphy of bats. side of each figure) is greatly elongated relative to those of the other digits. A. Rousettus amplexicaudatus (USNM 278616). B. Phyllostomus has- FETAL MEMBRANES tatus (AMNH 266071). Orientation of embryonic disc at time of implantation. Implantation of the embryo in the uterus generally occurs at the bilaminar blastocyst stage of embryonic development. primitive mammalian pattern. Interpreta- At the time of implantation, the embryonic tion of the pattern of transformation of this disc typically exhibits one of three orienta- character depends upon perceived relation- tions relative to the mesentery of the uterus ships among bats, primates, and other mam- (mesometrium). "Mesometrial" implanta- malian orders. The chiropteran condition, tion describes a condition in which the em- which is unique to bats among mammals, bryonic pole of the blastocyst is directed to- may represent a synapomorphy of bats. ward the mesometrium; implantation is Elongation of proximal phalanx of digit I termed "antimesometrial" when the abem- of foot. The proximal phalanx of pedal digit bryonic pole is directed toward the meso- I is less than or equal to the length of the metrium(Luckett, 1975, 1977, 1980b, 1993; proximal phalanges ofthe other digits in non- Mossman, 1987). "Orthomesometrial" ori- bat mammals. In contrast, the proximal pha- entation describes a condition in which an lanx of digit I in most bats is approximately axis running through the embryonic and 1.5 times longer than the proximal phalanges abembryonic poles is oriented at a 900 angle 1 994 SIMMONS: CHIROPTERAN MONOPHYLY 35 to the mesometrium (Luckett, 1975, 1977, described above exhibit either oftwo derived 1980b, 1993; Mossman, 1987). These pat- conditions: (1) paedomorphic retention ofan terns oforientation remain constant through- apparently absorptive bilaminar omphalo- out early development in all non-bat placen- pleure (e.g., phyllostomids and noctilionids), tal mammals regardless of differences in the or (2) formation of a trilaminar omphalo- degree of invasive activity that accompanies pleure without development of a free yolk implantation (Luckett, 1977, 1980b, 1993). sac, but with collapse and hypertrophy ofthe In megachiropterans and most microchi- yolk sac wall (e.g., megadermatids, thyrop- ropterans, the embryonic disc does not bear terids, vespertilionids; Luckett, 1980b, 1993). a constant orientation to one pole ofthe uter- Both ofthese conditions appear to be derived us. Instead, the disc appears to be directed from a developmental pattern that involved toward the tubo-uterine junction rather than differentiation of a free, glandlike yolk sac bearing a specific orientation to the site of (Luckett, 1993). Because development of a mesometrial attachment (Rasweiler, 1979; free, glandlike yolk sac appears to be primi- Luckett, 1980b, 1993). A few bats (vesper- tive for bats (and is unique to bats among tilionids, thyropterids, desmodontines) ex- mammals), development ofthis structure can hibit fixed antimesometrial implantation, but be interpreted as a synapomorphy of Chi- this appears to be a condition derived within roptera. Microchiroptera (Luckett, 1980, 1993). In this Preplacenta and early chorioallantoic pla- context, orientation of the embryonic disc centa diffuse or horseshoe-shaped, with de- toward the utero-tubal junction can be inter- finitive placenta reduced to a more localized preted as a synapomorphy of Chiroptera discoidal structure. The eutherian preplacen- (Luckett, 1980b, 1993). ta consists of a somewhat thickened layer of Differentiation of a free, glandlike yolk sac. trophoblast which forms where the maternal A free yolk sac forms early in development epithelium of the uterus has broken down. and is maintained as a simple, sacciform Maternal capillaries lie in close contact with structure throughout most ofgestation in the the trophoblast of the preplacenta, but no majority of mammals, including most insec- fetal vessels have yet formed within the tro- tivorans, dermopterans, and primates (Luck- phoblast (Mossman, 1987). The preplacenta ett, 1975, 1977; Mossman, 1987). This con- eventually becomes vascularized on part or dition is presumed to be primitive for all ofits fetal surface by the vascular allantois, mammals (Luckett, 1977). In megachirop- thereby establishing the definitive chorioal- terans and many microchiropterans (rhino- lantoic placenta (Luckett, 1980b; Mossman, pomatids, emballonurids, rhinolophids, mo- 1987). lossids) a free yolk sac forms (fig. 7A, B, D) Placental development among bats is but subsequently collapses to lie as a flattened unique in that it involves formation ofa broad sac over the surface ofthe definitive placental diffuse or horseshoe-shaped preplacenta and disc (Gopalakrishna, 1958; Luckett, 1980b, early chorioallantoic placenta, which is later 1993; Rasweiler, 1990, 1992). The endoder- reduced to form a more localized, discoidal mal cells of the yolk sac become hypertro- definitive placenta (fig. 7; Luckett, 1980b, phied, and the resulting yolk sac assumes a 1993; Rasweiler, 1990, 1992). A broad dif- unique "glandlike" appearance that is not seen fuse preplacenta also forms and is reduced in in other mammals (fig. 7C, E, F; Gopalak- hyracoids, but the definitive placenta is zo- rishna, 1958; Luckett, 1977, 1980b, 1993; nary rather than discoidal (Mossman, 1987). Mossman, 1987; Wible and Novacek, 1988; The pattern of early placental development Rasweiler, 1990, 1992). This complex ap- seen in bats occurs in no other group ofmam- parently stores glycogen and lipids that serve mals and thus may be considered a synapo- as an energy source just before parturition morphy ofChiroptera (Luckett, 1980b, 1993). (Stephans and Easterbrook, 1968; Rasweiler, Definitive chorioallantoic placenta endo- 1990; Luckett, 1993). Presence of a free, theliochorial. The degree of invasive activity glandlike yolk sac is unique to bats among of the definitive chorioallantoic placenta var- mammals (Luckett, 1980b, 1993). ies widely among mammals. Three major pla- Microchiropterans that fail to develop as cental types are recognized. An "epitheli- 36 AMERICAN MUSEUM NOVITATES NO. 3103

B E

GYS

Fig. 7. Stages in fetal membrane development in a megachiropteran bat (A-C) and microchiropteran bat (D-F); see text for discussion. The developmental stages shown for the two bats are not equivalent, but simply represent progressive stages in fetal development. The different stages in each sequence (e.g., A-C) have not been drawn to relative scale. A, B, C. Pteropus sp. (redrawn from Mossman, 1987: pl. 9). D, E, F. Molossus ater (redrawn from Rasweiler, 1992: figs. 18.6, 18.7, 18.9). A = allantois; CAP = definitive chorioallantoic placenta; GYS = glandular yolk sac; PP = preplacenta; YS = yolk sac. 1994 SIMMONS: CHIROPTERAN MONOPHYLY 37 ochorial" placenta is one in which there is no Mossman, 1937, 1987). Most strepsirhine loss of maternal tissue, so the chorionic tro- primates have an epitheliochorial placenta, phoblast is effectively separated from the ma- while other archontans (dermopterans, tar- ternal blood supply by at least two tissue lay- siers, and anthropoids) have a hemochorial ers (Luckett, 1977; Mossman, 1987). An placenta (Luckett, 1975, 1977, 1980b, 1993; "endotheliochorial" placenta forms when the Mossman, 1937, 1987). Although still the maternal epithelium and all or part of the source of some controversy (e.g., see Martin, underlying connective tissue are lost, result- 1990), it now appears that the epitheliochori- ing in apposition ofthe chorionic trophoblast al placenta is primitive for eutherian mam- and the maternal capillary endothelium mals and probably for Archonta and Pri- (Luckett, 1977; Mossman, 1987). Finally, a mates as well (Luckett, 1975, 1977, 1980b, "hemochorial" placenta is established when 1993; Mossman, 1987). all of the maternal tissue separating the ma- Luckett (1975, 1977, 1993) has argued that ternal blood from the trophoblast breaks there is no uniform shared pattern of fetal down, bathing the trophoblast in maternal membrane development among most taxa blood (Luckett, 1977; Mossman, 1987). with an endotheliochorial placenta, and thus Two placenta types occur in bats: endothe- that endotheliochorial placentation has liochorial and hemochorial. According to evolved convergently many times in mam- Luckett (1980b: 257), mals. Luckett (1993: 175) observed that ... careful consideration of all developmental Maternal capillary endothelium persists within features associated with endotheliochorial pla- the placenta and is separated from the syncy- centation ..., including fate of the polar tro- tiotrophoblast by a relatively thick, PAS-posi- phoblast, amniogenesis, patterns of implanta- tive lamina ("interstitial membrane") in the tion, and fate ofthe definitive yolk sac, suggests morphotype of the families Pteropodidae, Rhi- that an endotheliochorial placenta has devel- nopomatidae, Rhinolophidae, Emballonuridae, oped homologously in the chiropteran subor- Megadermatidae, and Noctilionidae. Both com- ders, but convergently in carnivorans and scan- parative and ontogenetic analyses suggest that dentians. this endotheliochorial relationship represents the primitive chiropteran condition. If bats are members of Archonta, then presence of an endotheliochorial placenta would be interpreted as a synapomorphy of bats. Some megachiropterans and members ofthe This feature was noted as a chiropteran syn- remaining microchiropteran families devel- apomorphy by Wible and Novacek (1988: op a hemochorial placenta, but this appears table 3), who described it as "prominent 'in- to be a condition that is secondarily derived terstitial membrane' in the chorioallantoic within bats (Luckett, 1980b, 1993). Data from placenta." It should be noted, however, that an ultrastructural study ofchanging tissue re- some workers consider an endotheliochorial lationships during ontogeny of the placenta placenta to be primitive for eutherian mam- in Myotis (Enders and Wimsatt, 1968) ap- mals (e.g., Martin, 1990), while others do not parently provide evidence for the transfor- believe that bats belong to a monophyletic mation of endotheliochorial to hemochorial Archonta (e.g., Stanhope et al., 1992, 1993). placentation (Luckett, 1980b, 1993). In this Under these interpretations, endotheliocho- context, it seems most likely that the prim- rial placentation may be either ambiguous or itive condition for bats is presence of an en- may represent a plesiomorphic condition. dotheliochorial placenta (Luckett, 1980b, 1993). Among non-bat eutherians, an endotheliochorial placenta is found in some edentates NERVOUS SYSTEM (bradypodids), some insectivorans (soricids, Cortical somatosensory representation of some talpids), tubulidentates, some rodents forelimb reverse of that in other mammals. (heteromyids), proboscideans, carnivorans, Somatic sensory input from various parts of scandentians, and two species of strepsirhine the body is received by specific areas of the primates (Luckett, 1975, 1977, 1980b, 1993; neocortex in mammals. "Somatotopic maps" 38 AMERICAN MUSEUM NOVITATES NO. 3103 of the primary somatosensory cortex (fig. 8) apomorphies that must be evaluated in terms may be obtained by systematically stimulat- of the observational methods employed, cri- ing sensors in different parts of the body and teria for homology, perceived levels of with- recording the pattern of electrical responses in- and among-taxon variation, and the phy- in the neocortex. These maps typically con- logenetic context in which a given feature is tain discrete representations ofthe body sur- interpreted. There are numerous reasons why face. Somatotopic maps of primary somato- a putative synapomorphy may be validly re- sensory cortex reveal a similar orientation of jected. forelimb representation in most mammals, Perhaps the most basic reason for rejecting with the distal elements of the forelimb oc- a synapomorphy is simple observational er- curring rostral to more proximal elements in ror, when taxa have been cited as having a the somatotopic map (fig. 8E). This relative feature that they do not actually exhibit, or orientation of the forelimb representation is lacking a feature that is clearly present. Pu- seen in monotremes, marsupials, and all non- tative synapomorphies in such cases may be bat taxa studied thus far (Bohringer and Rowe, found to apply at higher or lower taxonomic 1977; Kaas, 1983; Wible and Novacek, 1988). levels than originally reported, or they may Somatotopic maps have been compiled for be rendered ambiguous when the observa- only three bats. In one microchiropteran tional data are corrected. This can also occur (Macroderma) and one megachiropteran when additional sampling indicates that a (Pteropus), somatosensory forelimb repre- distribution originally inferred for a character sentations are the reverse ofthat ofthe body, (e.g., uniform presence in a given family or which maintains the same relative position order) is incorrect. In some cases, more de- as seen in somatotopic maps of other mam- tailed sampling within groups may document mals (fig. 8C, D; Calford et al., 1985; Wise levels ofwithin-group variation that meet or et al., 1986). This arrangement is apparently exceed the amount ofamong-group variation unique among mammals. Pettigrew et al. originally perceived. This variation may re- ( 1 989) stated that one microchiropteran (An- sult in such ambiguity that evolutionary in- trozous) lacks this reversal of the forelimb terpretation of a character becomes impos- representation, and cited Zook and Fowler sible, leading to rejection of the feature as a (1982) and Zook (personal commun.) as the phylogenetic character at the taxonomic level sources of this information. However, data under consideration. supporting this claim have never been pub- Other reasons for rejecting putative syn- lished. Contra Pettigrew et al. (1989), Zook apomorphies involve definition and homol- and Fowler's (1982) publication, which is an ogy of the features in question. Some char- abstract, contains no mention of forelimb acters have been defined in vague terms that orientation. Kaas (personal commun.) has suggest but do not support a hypothesis of seen the summary diagrams of Zook and homology (e.g., "derived, non-insectivorous Fowler, and reports that they show the same dentition" cited by Smith and Madkour, forelimb orientation in Antrozous as seen in 1980). If further comparisons or develop- other bats. Given the data currently avail- mental data indicate that non-homologous able, it seems likely that reversal ofthe fore- conditions have been lumped together under limb representation represents another syn- such a description (as in this case; Koopman apomorphy of bats. and Maclntyre, 1980), the character may be rejected on the grounds that it fails an initial test of similarity, a prerequisite for homol- REJECTED PUTATIVE ogy. Such character descriptions are, essen- tially, too superficial to be phylogenetically SYNAPOMORPHIES informative. Recognition of phylogenetic relationships Finally, a critical component of character and identification of synapomorphies is an interpretation is the phylogenetic context. The iterative process, and disagreements con- position of a clade in the phylogenetic tree cerning conclusions are common. Systema- may strongly affect hypotheses of synapo- tists are often faced with lists ofputative syn- morphy. For example, a particular character 1 994 SIMMONS: CHIROPTERAN MONOPHYLY 39

CAUDAL

MEDIAL B D( z

Fig. 8. Cortical representations of the body surface as determined from somatosensory mapping experiments; see text for discussion. All ofthe figures shown here were redrawn from Wise et al. (1986). A. Body surface "map" reconstructed from receptive field data collected from two specimen's of the microchiropteran bat Macroderma gigas. B. Approximate location of the body surface map (A) in the brain of Macroderma gigas. C. Schematic representation (homunculus) of the body surface of Macro- derma gigas. Compare this homunculus with the cortical map in figure A, from which it was derived. D. Schematic representation ofthe body surface ofa megachiropteran bat, Pteropus poliocephatus (from Calford et al., 1985). E. Schematic representation of the body surface of a laboratory rat (from Kaas, 1983). Note that the digits of the forelimb are directed caudally in both bats (C, D), but are directed rostrally in the rat (E). 40 AMERICAN MUSEUM NOVITATES NO. 3103 may appear to be a synapomorphy of bats if ophids and phyllostomids possess the intra- they nest within Archonta, but may be in- cranial vessel. An intracranial vessel similar terpreted as plesiomorphic if bats fall else- to that seen in bats is present in some sori- where in the mammalian family tree. When comorph insectivorans, but other sorico- homoplasy is evident in a character, the iden- morphs and erinaceomorphs lack this vessel tity of successive sister taxa may greatly in- (Roux, 1947). This distribution pattern led fluence evolutionary interpretation. If a de- Wible and Novacek (1988) to conclude that rived state is present in a clade but absent in an extracranial ramus infraorbitalis is prim- at least two successive sister taxa, that con- itive for insectivorans. Accordingly, the in- dition can be interpreted as a synapomorphy tracranial vessel seen in bats appears to be of the clade in question even if the derived independently derived, and presence of this state appears in other taxa in the tree. It is vessel was interpreted as a chiropteran syn- not appropriate to reject a putative synapo- apomorphy by Wible and Novacek (1988). morphy simply because a similar condition Recognition of the intracranial ramus in- appears in another taxon; the phylogenetic fraorbitalis as a synapomorphy of bats as- relationships among outgroup taxa must be sumes that this vessel is absent in the sister considered. taxa of bats. This appeared to be true at the Several characters previously cited as chi- time of Wible and Novacek's (1988) study, ropteran synapomorphies do not appear to but that is no longer the case: Wible (1993) be valid under closer inspection, given the recently noted that an intercranial ramus in- assumptions of this study. Reasons for re- fraorbitalis is present in juvenile dermopter- jecting each putative synapomorphy are dis- ans. If bats and dermopterans are sister taxa cussed below. as suggested by Novacek and Wyss (1986), Ramus infraorbitalis ofthe stapedial artery Wible and Novacek (1988), Novacek (1986, passes through the cranial cavity dorsal to 1990, 1992a), Johnson and Kirsch (1993), the alisphenoid. Wible and Novacek (1988) Szalay and Lucas (1993), Simmons (1993, in cited an intracranial course of the ramus in- prep.), and Wible (1993), then presence ofan fraorbitalis of the stapedial artery as a syn- intracranial ramus infraorbitalis cannot be apomorphy of bats. The majority of euther- considered a synapomorphy of bats. Rather, ian mammals exhibit one oftwo extracranial it apparently applies at a higher taxonomic courses: passage through the orbitotemporal level-that of Volitantia (Dermoptera + region ventral to the alisphenoid, or passage Bats). through a canal in the alisphenoid (Wible, Lesser tuberosity ofhumerus projects prox- 1987, 1993; Wible and Novacek, 1988). Based imally beyond the level of the articular sur- on the distribution of these states, Wible face of the humeral head. The lesser tuber- (1987, 1993) and Novacek (1986) argued that osity of the humerus is often called the passage ventral to the alisphenoid is primi- "trochin" in bats. Beard (1993a) indicated tive for Eutheria. In contrast, in bats the ra- that projection of this structure beyond the mus infraorbitalis has an intracranial course level of the articular surface of the humeral which passes through the orbitotemporal re- head is a synapomorphy of Chiroptera. This gion dorsal to the alisphenoid (Wible and No- condition stands in contrast to that seen in vacek, 1988; Wible, 1993). This intracranial most mammals, where the lesser tuberosity vessel is apparently not homologous with the of the humerus does not extend beyond the extracranial ramus infraorbitalis of other level ofthe humeral head (Beard, 1993a; per- mammals because both vessels occur in some sonal obs.). microchiropterans (Buchanan and Arata, While projection of the lesser tuberosity 1967; Wible and Novacek, 1988). beyond the humeral head is clearly derived, Kallen (1977) indicated that the intracra- Beard's (1993a) interpretation ofthis feature nial ramus infraorbitalis is absent in at least appears to be incorrect. The lesser tuberosity two bat taxa, Rhinolophus (Rhinolophidae) does not extend beyond the articular surface and Desmodus (Phyllostomidae). Wible and of the humeral head in many microchirop- Novacek (1988) interpreted this as a second- terans (e.g., Balantiopteryx, Thyroptera, Mo- arily derived condition because other rhinol- lossus; Smith, 1972: fig. 6) nor in any mega- 1 994 SIMMONS: CHIROPTERAN MONOPHYLY 41 chiropterans (Vaughan, 1970a: fig. 13; in pteropines and rhinolophines, but my ex- personal obs.). Projection of the lesser tuber- amination of specimens suggests that the pi- osity ofthe humerus beyond the head appears siform in these forms is present but may be to be a condition derived within Microchi- fused to the magnum. In this context, absence roptera, and thus cannot be a synapomorphy of the pisiform cannot be considered a syn- of bats. apomorphy of bats. 900 rotation of manus. Wible and Novacek Dorsal ischia meet above vertebral axis. (1988: table 3) listed "manus rotated 900 from Orientation ofthe pelvis such that the dorsal position typical for quadrupedal mammals" ischia meet above the vertebral axis was list- as a synapomorphy of bats. In quadrupedal ed as a possible synapomorphy of bats by mammals the axis of flexion of the proximal Baker et al. (199 lb: table 1). While this con- wrist joint lies roughly parallel to the axis of dition is indeed seen in a few megachirop- flexion of the elbow during normal locomo- terans and microchiropterans, my examination. This presumably represents the primi- tion of skeletal material indicates that it is tive condition for mammals. Morphology of not found in the majority of taxa in either the wrist and elbow in cursorial mammals suborder. When the derived condition is precludes rotation of the manus, effectively present (e.g., in Pteropus), variation exists locking the axis of flexion of the manus into even within species. For example, the dorsal the parallel position. In bats, similar modi- ischia meet above the axis of the vertebral fications of the elbow and reduction of the column in male Pteropus tonganus (e.g., distal ulna lock the manus into a fixed po- USNM 546349), but not in females of the sition relative to the elbow, but the axis of same species (e.g., USNM 546347). Accord- flexion of the proximal wrist joint lies at an ingly, this character does not appear to rep- angle approximately 900 to that ofthe elbow. resent a valid synapomorphy of bats. This modification is the result of relative Iliosacral fusion involving last lumbar ver- twisting ofthe distal end ofthe radius, which tebra. Involvement of the last lumbar ver- has realigned the axis ofthe radiocarpal facets tebra in the iliosacral fusion was listed by so that it is perpendicular (rather than par- Baker et al. (1991b: table 1) as a possible allel) to the axis offlexion ofthe elbow. While synapomorphy of bats. This character is this is clearly a derived condition, it is not problematic from several perspectives. First, unique to bats-dermopterans exhibit the the distinction between "sacral" and "lum- same modifications. If bats and dermopter- bar" vertebrae is typically based on presence/ ans are sister taxa, then this derived character absence of participation in the joint between cannot be considered a synapomorphy ofbats. the ilium and the vertebral column. In evo- Rather, it apparently applies at a higher tax- lutionary terms, a vertebra may be trans- onomic level-that of Volitantia. formed from a lumbar to a sacral vertebra by Absence of pisiform. Beard (1993a) stated establishment of a joint with the ilium and that the pisiform is absent in bats, and in- fusion with the other sacral vertebrae. In some terpreted this as a synapomorphy of Chirop- cases it may be recognized as a homolog of tera. If the pisiform were absent, this inter- the last lumbar vertebrae of other taxa, but pretation would be correct; however, the such homologies are hard to establish when pisiform is present in both microchiropteran vertebral counts are taxonomically variable. and megachiropteran bats (Dobson, 1878; In bats, the number ofthoracic, lumbar, and Vaughan, 1959, 1970a; Jepsen, 1966, 1970; sacral vertebrae varies considerably among Altenbach, 1979; personal obs.). Although species. For example, Walton and Walton concealed in dorsal views of the wrist, a ro- (1970: table 1) noted 11-14 thoracic verte- bust, rodlike pisiform extends obliquely brae, 4-6 lumbar vertebrae, and 3-6 sacral across the posteroventral surface of the chi- vertebrae in different bat taxa. Unfortunate- ropteran carpus, where it is tightly bound by ly, the total number of vertebrae in the tho- ligaments to the cuneiform, magnum, and racic through sacral series also varies among trapezium (Vaughan, 1959, 1970a; Alten- bats (from 19-24; Walton and Walton, 1970), bach, 1979: fig. 31; personal obs.). Allen so evolutionary subtraction ofvertebrae from (1893) noted that the pisiform may be absent one part of the series (e.g., lumbar) does not 42 AMERICAN MUSEUM NOVITATES NO. 3103 necessarily mean that homologs ofthose ver- nose Chiroptera (table 4). The fact that these tebrae have been added to another part ofthe features represent many different anatomical vertebral series (e.g., thoracic or sacral). This systems (dentition, skull, cranial vasculature makes it very difficult to assess homologies system, postcranial musculoskeletal system, of vertebra associated with the iliosacral fu- fetal membranes, nervous system) further sion. strengthens the case for bat monophyly. Even if the character description in Baker The degree of character support for Chi- et al. (1991 b) is interpreted as indicating that roptera compares favorably with perceived the last lumbar can be recognized as such support for other mammalian groups that are (e.g., it forms a contact with the ilium but is generally agreed to be monophyletic. Theria, not yet fully fused to the sacral vertebrae), Eutheria, Primates, Carnivora, Perissodac- there are still problems with this character. tyla, Sirenia, and Proboscidea are each di- Most importantly, in most megachiropterans agnosed by 6-10 morphological synapomor- and microchiropterans there is no contact be- phies, fewer than halfthe number offeatures tween the last lumbar vertebrae (sensu lato) that diagnose Chiroptera (Novacek, 1990; and the ilium. The first vertebra that artic- Beard, 1993a; Fischer and Tassy, 1993; Wyss ulates with the ilium is typically highly mod- and Flynn, 1993). In the E-globin sequence, ified, with transverse processes that extend over 30 derived substitutions diagnose Chi- the full length ofthe centrum and contact the roptera, while only 4 such substitutions di- ilium along their entire length. The centrum agnose Primates (Bailey et al., 1992). Alter- and transverse processes are completely fused natively, Primates is diagnosed by 18 with those of the succeeding sacral vertebra, transversions in the COII data set, while Chi- suggesting that the first vertebra involved in roptera and Artiodactyla are each diagnosed the iliosacral joint should be considered a by 6-7 transversions (Adkins and Honeycutt, "true" sacral vertebra sensu Flower (1885). 1993). While measurements ofbranch length In a few instances a case may be made for clearly depend on taxonomic sampling, tree incorporation of the last lumbar into the il- topology, and methods used to define char- iosacral fusion in a particular specimen, but acters (see discussion below), comparisons of the evidence supporting this conclusion is relative character support nevertheless sug- based on comparisons of sacral morphology gest that Chiroptera is one of the better sup- within the species, not among higher taxa. In ported clades within Mammalia. this context, inclusion ofthe last lumbar ver- From the conclusion that bats are mono- tebra in the iliosacral fusion does not appear phyletic it follows that wings and powered to be a valid synapomorphy of bats. flight evolved only once in mammals. As discussed earlier, the oldest known fossil bats are fully volant microchiropterans from the DISCUSSION AND CONCLUSIONS Early Eocene; megachiropteran bats first ap- The molecular and morphological data pear in the fossil record in the Late Eocene currently available strongly support bat (Jepsen, 1966; Van Valen, 1979; Habersetzer monophyly. Although some characters are and Storch, 1987; Novacek, 1987; Ducrocq difficult to interpret, a large number of pu- et al., 1993). Given these dates, it seems likely tative chiropteran synapomorphies have been that flight evolved in the chiropteran lineage proposed. For example, 39 derived substi- sometime in the Paleocene or even the Late tutions in the e-globin sequence, 22 derived Cretaceous, 58-70 million years ago. More substitutions in the IRBP sequence, 8 derived precise estimates will depend upon increased substitutions in the 12S rDNA sequence, and resolution ofthe branching pattern ofthe var- 7 derived substitutions in the COII sequence ious eutherian orders. apparently diagnose Chiroptera (Adkins and Honeycutt, 1991, 1993; Ammerman and Hillis, 1992, Bailey et al., 1992; Stanhope et WHAT IS THE SISTER GROUP OF BATS? al.,, 1992, 1993). Over 25 morphological syn- Critical questions remain concerning the apomorphies-many of which consist of place of bats within Eutheria. While most complex suites of modifications-also diag- workers now agree that bats are monophy- 1 994 SIMMONS: CHIROPTERAN MONOPHYLY 43

TABLE 4 Morphological Synapomorphies of Chiropteraa

1) Deciduous dentition does not resemble adult den- 14) Modification of hip joint: 900 rotation ofhindlimbs tition; deciduous teeth with long, sharp, recurved effected by reorientation ofacetabulum and shaft of cusps. femur; neck of femur reduced; ischium tilted dor- 2) Palatal process ofpremaxilla reduced; left and right solaterally; anterior pubes widely flared and pubic incisive foramina fused in midsagittal plane. spine present; absence of m. obturator intemus. 3) Postpalatine torus absent. 15) Absence of m. gluteus minimus. 4) Jugal reduced and jugolacrimal contact lost. 16) Absence of m. sartorius. 5) Two entotympanic elements in the floor ofthe mid- 17) Vastus muscle complex not differentiated. dle-ear cavity: a large caudal element, and a small 18) Modification of ankle joint: reorientation of upper rostral element associated with the internal carotid ankle joint facets on calcaneum and astragalus; artery. trochlea of astragalus convex, lacks medial and lat- 6) Tegman tympani tapers to an elongate process that eral guiding ridges; tuber of calcaneum projects in projects into the middle-ear cavity medial to the plantolateral direction away from ankle and foot; epitympanic recess. peroneal process absent; sustentacular process of 7) Proximal stapedial artery enters cranial cavity me- calcaneum reduced, calcaneoastragalar and susten- dial to the tegmen tympani; ramus inferior passes tacular facets on calcaneum and astragalus coa- anteriorly dorsal to the tegmen tympani. lesced; absence of groove on astragalus for tendon 8) Modification of scapula: reorientation of scapular of m. flexor digitorum fibularis. spine and modification of shape of scapular fossae; 19) Presence of calcar and depressor ossis styliformes reduction in height of spine; presence of a well-de- muscle. veloped transverse scapular ligament. 20) Entocuneiform proximodistally shortened, with flat, 9) Modification of elbow: reduction of olecranon pro- triangular distal facet. cess and humeral articular surface on ulna; presence 21) Elongation of proximal phalanx of digit 1 of foot. of ulnar patella; absence of olecranon fossa on hu- 22) Embryonic disc oriented toward tubouterine junc- merus. tion at time of implantation. 10) Absence of supinator ridge on humerus. 23) Differentiation of a free, glandlike yolk sac. 11) Absence of entepicondylar foramen in humerus. 24) Preplacenta and early chorioallantoic placenta dif- 12) Occipitopollicalis muscle and cephalic vein present fuse or horseshoe-shaped, with definitive placenta in leading edge of propatagium. reduced to a more localized discoidal structure. 13) Digits II-V offorelimb elongated with complex car- 25) Definitive chorioallantoic placenta endotheliocho- pometacarpal and intermetacarpal joints, support rial. enlarged interdigital flight membranes (patagia); 26) Cortical somatosensory representation of forelimb digits III-V lack claws. reverse of that in other mammals. a See text for discussion.

letic, there is no agreement concerning the and at least one morphological data set (e.g., identity of the sister taxon of bats. Mono- Cronin and Sarich, 1980; Miyamoto and phyly ofArchonta-a clade supposed to con- Goodman, 1986; Bailey et al., 1992; Kay et tain bats, dermopterans, primates, scanden- al., 1992; Stanhope et al., 1992,1993; Adkins tians, and several fossil taxa-has been and Honeycutt, 1993; Honeycutt and Ad- supported by many studies based on mor- kins, 1993; Sarich, 1993). Numerous clades phological data (e.g., Smith and Madkour, of both archontan and non-archontan mam- 1980; Novacek and Wyss, 1986; Novacek, mals have been proposed as the sister group 1986, 1990, 1992a, in press; Wible and No- of bats (table 5). In this context, it is very vacek, 1988; Greenwald, 1991; Johnson and difficult to establish just which morphologi- Kirsch, 1993; Szalay and Lucas, 1993) and cal features (or nucleotide substitutions) are combined morphological and molecular data chiropteran synapomorphies. Many unique (Novacek, 1994). However, archontan characteristics of bats, such as morphology monophyly has been rejected in other studies ofthe deciduous dentition, would be consid- based on analyses ofbiochemical, molecular, ered synapomorphies under any hypothesis 44 AMERICAN MUSEUM NOVITATES NO. 3103 that accepts chiropteran monophyly. How- with each other than Chiroptera shares with ever, interpretation of other features varies any of its putative sister taxa. How can we according to the identity of the sister group account for this pattern, and also for the di- of bats.3 versity ofopinions concerning the identity of One source of confusion concerning chi- the sister group of bats? Although there are ropteran relationships has been uneven tax- problems associated with any supposition of onomic sampling. Many relevant studies have clocklike evolutionary change (Scherer, 1990), included only a few taxa, thus groups iden- one explanation for the pattern of synapo- tified as the sister taxon ofbats in some anal- morphies is that the temporal length of the yses (e.g., Carnivora; Stanhope et al., 1992) common ancestral lineage shared by bats and were not even considered in other studies (e.g., their sister taxon was very short compared Adkins and Honeycutt, 1991, 1993; Am- to the subsequent period of divergence. An- merman and Hillis, 1992; Bailey et al., 1992; other possibility is that evolution occurred Kay et al., 1992). Those morphological stud- unusually rapidly in the bat lineage subse- ies that included data from all or most of the quent to its separation from its sister lineage. mammalian orders have uniformly identified Neither ofthese hypotheses can be addressed Dermoptera as the sister group of bats (e.g., until the relationship of Chiroptera to other Novacek and Wyss, 1986; Novacek, 1986, mammalian clades has been resolved. 1990, 1992; Wible and Novacek, 1988; Greenwald, 1991; Johnson and Kirsch, 1993). DIREcTIONS FOR FUTURE RESEARCH In contrast, conclusive molecular studies with Given the compelling evidence which now comparable taxonomic sampling-all of supports monophyly of Chiroptera, it seems which have relied on protein amino acid se- clear that future studies of higher-level rela- quence data-have identified the sister taxon tionships of bats should concentrate on re- ofbats as a larger clade including some com- solving the position of bats within Eutheria bination of Scandentia, Insectivora, Carniv- (and relationships within the two bat sub- ora, Pholidota, and Tubulidentata (Miya- orders) rather than continuing to focus on bat moto and Goodman, 1986; Stanhope et al., monophyly. While data relevant to bat 1993). Of particular importance is the fact monophyly will always be of interest, it is was in of that Dermoptera not included any time to move beyond this controversy to in- these studies. vestigate evolutionary problems at other tax- Examination of branch lengths in trees onomic levels. based on analyses ofmolecular data (e.g., Ad- kins and Honeycutt, 1991, 1993; Stanhope Future studies directed toward resolving Wi- the relationships of Chiroptera to other or- et al., 1992, 1993) and morphology (e.g., ders should include several components. In- ble and Novacek, 1988; Simmons, 1993) increased taxonomic sampling in the context dicates that only a few putative synapomor- of some data subsets may prove particularly phies link bats with any other eutherian order. is clear that Megachiroptera and Micro- productive. Analyses of nucleotide sequence It data hold great promise, but few studies to chiroptera share far more synapomorphies date have included representatives of more than half of the extant orders. As demon- 3 It should be noted that alternative hypotheses of sis- strated by Adkins and Honeycutt's (1991, ter-group relationships may increase perceived character 1993) analyses of COII sequence data, ad- support for chiropteran monophyly. For example, in this dition of a few taxa can significantly affect study I have tentatively accepted Dermoptera as the sis- the outcome of a study. Future research inter group of bats (see Morphological Characters Sup- volving broad sampling of mammalian or- porting Bat Monophyly). Accordingly, derived morphological traits shared by dermopterans and bats have been ders may be expected to reveal phylogenetic interpreted as synapomorphies ofVolitantia, from which patterns not seen in previous studies. How- it follows that they must be plesiomorphic for Chirop- ever, use of single species as exemplars of tera. If Dermoptera and Chiroptera are not sister taxa, diverse orders should be avoided, as artifacts however, these features may have evolved independently ofwithin-group variation may affect the out- in the two lineages, and thus may be added to the list of come of analyses of among-group relation- possible synapomorphies of Chiroptera. ships. 1994 SIMMONS: CHIROPTERAN MONOPHYLY 45

TABLE 5 Proposed Sister Group of Chiroptera Sister clade Study Type of data Dermoptera Gregory (1910); Novacek and Wyss Morphological (1986); Novacek (1986, 1990, 1992a); Wible and Novacek (1988); Greenwald (1991); Johnson and Kirsch (1993); Simmons (1993); Szalay and Lucas (1993); Wible (1993) Novacek (1994) Morphological + mole- culara Dermoptera + Primates Beard (1993a, 1993b) Morphological Primates + Scandentia Kay et al. (1992) Morphological Dermoptera + Primates + Scan- Ammerman and Hillis (1992) Molecular dentiab Dermoptera + Primates + Scan- Bailey et al. (1992) Molecular dentia + Lagomorphac Scandentia + Insectivora + Car- Miyamoto and Goodman (1986) Moleculare nivora + Pholidotad Insectivora (excluding Erinaceus) Stanhope et al. (1993) Molecularf + Tubulidentatad Insectivora + Carnivorad Stanhope et al. (1993) Molecularg Carnivora Stanhope et al. (1992, 1993) Molecularh Artiodactyla1 Adkins and Honeycutt (1993) Molecular a The data set included 49 morphological characters and information from 684 base pairs of the COII gene. An analysis including the morphological data plus all substitutions in the COII data could not resolve the sister group of bats. Dermoptera was identified as the sister group in an analysis that included morphological data and COII transversions only. b Archonta was assumed to be monophyletic in the analysis. c The only other taxon included in this study was Artiodactyla, which was used as an outgroup. d Dermoptera was not included in the study. e Combined protein data set including amino acid sequence data from a- and ,3-globins, myoglobins, lens aA crystallins, fibrinopeptides, cytochrome c, and ribonucleases. fAmino acid sequence data from a - and ,B-globins. 5 Combined protein data set including amino acid sequence data from a- and f3-globins, myoglobins, lens aA crystallins, fibrinopeptides, cytochrome c, ribonucleases, and embryonic a- and f3-globins. h RBP data. i The most parsimonious tree was rooted through an edentate; Carnivora and Insectivora were not included in the study.

When multiple representatives of orders uate eutherian relationships in the context of are included in a study, it may be useful to ordinal monophyly. This omission is unfor- constrain some analyses to preserve ordinal tunate since there is strong evidence from or subordinal monophyly to facilitate inves- other data sets that each of these groups is tigation ofrelationships among these groups. monophyletic (Prothero et al., 1988; Honey- Springer and Kirsch (1993) included several cutt and Adkins, 1993; Luckett and Harten- artiodactyls, rodents, and bats in their study berger, 1993; Simmons, 1993, this paper). in order to test monophyly of these orders, The importance of fossils for understand- but never ran constrained analyses to eval- ing higher-level relationships ofmammals has 46 AMERICAN MUSEUM NOVITATES NO. 3103 been highlighted in several studies (e.g., Beard, descriptions and interpretations ofbiological di- 1990, 1993a; Novacek, 1990, 1992a, 1992b). versity than those that focus on just one approach." Although phylogenetic studies including extinct taxa are often plagued by missing data, Integrated studies that include morpholog- the information preserved in such taxa may ical data from many organ systems-and mo- be crucial for understand relationships among lecular data from many genes and proteins- extant forms. Studies by Beard (1990, 1993a) may hold the key to unraveling eutherian re- and Kay et al. (1992) have demonstrated that lationships, including the positions of Chi- extinct paromomyids and plesiadapids should roptera and Primates. Continuing efforts to be considered in phylogenetic studies of ar- identify new character sets, fill sampling gaps, chontan mammals. and refine analytical methods should be en- A potentially productive method for re- couraged in hope that future studies will resolving bat relationships may be to combine solve the persistent problems of mammalian various data subsets in a "total evidence" phylogeny. approach (Kluge, 1989; Jones et al., 1993). Different subsets ofmorphological characters ACKNOWLEDGMENTS have been routinely combined in phylogenetic analyses relevant to bat relationships This study grew out of work that I began (e.g., Luckett, 1980b, 1993; Smith and Mad- as a Kalbfleisch-Hoffman Research Fellow at kour, 1980; Wible and Novacek, 1988; John- the American Museum ofNatural History in 1989-1991. M. Novacek and R. MacPhee son and Kirsch, 1993; Simmons, 1993), but most molecular studies have focused on only were instrumental in encouraging me to pur- a single gene or protein (e.g., Adkins and sue this line of enquiry, and I am grateful to Honeycutt, 1991, 1993; Ammerman and them for their support. Thanks also to T. Hillis, 1992; Bailey et al., 1992). Although Griffiths, K. Koopman, M. Novacek, A. Pef- some workers have combined different sub- fley, R. Van Den Bussche, R. Voss, P. Vrana, sets of molecular data (e.g., Czelusniak et al., and J. Wible for generously reading earlier 1990; Honeycutt and Adkins, 1993), taxo- versions ofthis manuscript and offering many nomic sampling has been a problem because helpful comments. P. Wynne provided the different data subsets typically sample sig- illustrations, and I thank her for her expertise nificantly different sets of taxa. Only one at- and patience. The analysis of postcranial tempt has been made to combine morpho- characters and preparation ofthe manuscript logical and molecular character data in a single were supported by National Science Foun- analysis (i.e., Novacek, 1994). dation Grant BSR-9106868. Studies combining molecular and morphological data are of particular interest when different data sets produce significantly dif- REFERENCES ferent phylogenies. Although there is some concern that information may be lost when Adkins, R. M., and R. L. Honeycutt data sets are combined, and that large mo- 1991. Molecular phylogeny of the superorder lecular data sets may "swamp out" the signal Archonta. Proc. Natl. Acad. Sci. U.S.A. from smaller morphological data sets, pre- 88: 10317-10321. liminary results of total evidence analyses 1993. A molecular examination of archontan have been promising (e.g., Novacek, 1994). and chiropteran monophyly. In R. D. E. MacPhee (ed.), Primates and their Jones et al. (1993: 100) observed recently that relatives in phylogenetic perspective, pp.

... arguments regarding conflicts between mo- 227-249. Advances in primatology se- lecular and morphological data are overstated. ries. New York: Plenum Press.

... Rather than increasing uncertainty in phy- Allen, H. logenetic inference, we see total evidence as 1893. A monograph of the bats of North maximizing descriptive and explanatory power. America. Bull. U.S. Natl. Mus. 43: 1- As Moritz and Hillis (1990: 4) pointed out, 198. "studies that incorporate both molecular and Altenbach, J. S. morphological data will provide much better 1979. Locomotor morphology of the vampire 1994 SIMMONS: CHIROPTERAN MONOPHYLY 47

bat, Desmodus rotundus. Am. Soc. motor areas ofthe cerebral cortex in the Mammal. Spec. Publ. 6: 1-137. platypus (Ornithorhynchus anatinus). J. Ammerman, L. K., and D. M. Hillis Comp. Neurol. 174: 1-14. 1992. A molecular test of bat relationships: Buchanan, G. D., and A. A. Arata monophyly or diphyly? Syst. Biol. 41: 1967. Cranial vasculature of a neotropical 222-232. fruit-eating bat, Artibeus lituratus. Anat. Anderson, K. Anz. 124: 314-325. 1912. Catalogue of the Chiroptera in the col- Buttery, R. G., J. R. Haight, and K. Bell lection of the British Museum, second 1990. Vascular and avascular retinae in mam- edition, volume I: Megachiroptera. mals: a funduscopic and fluorescein an- Trustees of the British Museum, Lon- giographic study. Brain Behav. Evol. don. 35(3): 156-175. Bailey, W. J., J. L. Slightom, and M. Goodman Calford, M. B., M. L. Graydon, M. F. Huerta, J. 1992. Rejection of the "flying primate" hy- L. Kaas, and J. D. Pettigrew pothesis by phylogenetic evidence from 1985. A variant of the mammalian somato- the e-globin gene. Science 256: 86-89. topic map in a bat. Nature 313: 477- Baker, R. J., R. L. Honeycutt, and R. A. Van Den 479. Bussche Campbell, C. B. G. 199 la. Examination of monophyly of bats: re- 1980. The nervous system of the Tupaiidae: striction map of the ribosomal DNA its bearing on phyletic relationships. In cistron. In T. A. Griffiths and D. Klin- W. P. Luckett (ed.), Comparative biol- gener (eds.), Contributions to mam- ogy and evolutionary relationships of malogy in honor of Karl F. Koopman. tree shrews, pp. 219-242. New York: Bull. Am. Mus. Nat. Hist. 206: 42-53. Plenum Press. Baker, R. J., M. J. Novacek, and N. B. Simmons Carleton, M. D., and G. G. Musser 199 lb. On the monophyly of bats. Syst. Zool. 1984. Muroid rodents. In S. Anderson and J. 40: 216-231. K. Jones (eds.), Orders and families of Barnes, L. G., and E. D. Mitchell recent mammals of the world, pp. 289- 1978. Cetacea. In V. J. Maglio and H. B. S. 379. New York: Wiley. Cooke (eds.), Evolution of African Carroll, R. L. mammals, pp. 582-602. Cambridge, 1988. Vertebrate paleontology and evolution. MA: Harvard Univ. Press. New York: W. H. Freeman. Beard, K. C. Coues, E. 1990. Gliding behavior and palaeoecology of 1872. Osteology and myology of Didelphys the alleged primate family Paromomyi- virginiana. Mem. Boston Soc. Nat. Hist. dae (Mammalia, Dermoptera). Nature 2: 41-154. 345: 340-341. Cronin, J. E., and V. M. Sarich 1993a. Phylogenetic systematics of the Prima- 1980. Tupaiid and archontan phylogeny: the tomorpha, with special reference to macromolecular evidence. In W. P. Dermoptera. In F. S. Szalay, M. J. No- Luckett (ed.), Comparative biology and vacek, and M. C. McKenna (eds.), evolutionary relationships of tree Mammal phylogeny: placentals, pp. shrews, pp. 293-312. New York: Ple- 129-150. Berlin: Springer-Verlag. num Press. 1993b. Origin and evolution ofgliding in Early Czelusniak, J., M. Goodman, B. F. Koop, D. A. Cenozoic Dermoptera (Mammalia, Pri- Tagle, J. Shoshani, G. Braunitzer, T. K. matomorpha). In R. D. E. MacPhee Kleinschmidt, W. W. de Jong, and G. Matsuda (ed.), Primates and their relatives in 1990. Perspectives from amino acid and nu- phylogenetic perspective, pp. 63-90. cleotide sequences on cladistic relation- Advances in primatology series. New ships among higher taxa ofEutheria. In York: Plenum Press. H. Genoways (ed.), Current mammal- Benton, M. J. ogy 2: 545-572. New York: Plenum 1990. Phylogeny ofthe major tetrapod groups: Press. morphological data and divergence Dal Piaz, G. dates. J. Mol. Evol. 30: 409-424. 1937. I. Mammiferi dell'Oligocene veneto. Blumenbach, J. F. Archaeopteropus transiens. Mem. Inst. 1779. Handbuch der Naturgeschicht. Geol., Univ. Padova 11: 1-8. Bohringer, R. C., and M. J. Rowe de Jong, W. W., J. A. M. Leunissen, and G. J. 1977. The organization of the sensory and Wistow 48 AMERICAN MUSEUM NOVITATES NO. 3103

1993. Eye lens crystallins and the phylogeny M. J. Novacek, and M. C. McKenna ofplacental orders: evidence for a mac- (eds.), Mammal phylogeny: placentals, roscelid-paenungulate clade? In F. S. pp. 217-234. Berlin: Springer-Verlag. Szalay, M. J. Novacek, and M. C. Mc- Fleischer, G. Kenna (eds.), Mammal phylogeny: pla- 1973. Studien am Skelett des Gehororgans der centals, pp. 5-12. Berlin: Springer-Ver- Saiugetiere, einschliel3lich des Men- lag. schen. Saiugk. Mitt. (Miinchen) 21: Dobson, G. E. 1131-1239. 1875. Conspectus of the suborders, families 1978. Evolutionary principles of the mam- and genera of Chiroptera arranged ac- malian middle ear. Adv. Anat. Em- cording to their natural affinities. Ann. bryol. Cell Biol. 55: 5-67. Mag. Nat. Hist., Ser. 4, 16: 345-357. Flower, W. H. 1878. Catalogue of the Chiroptera in the col- 1885. An introduction to the osteology of the lection ofthe British Museum. London: Mammalia, 3rd ed. London: MacMil- British Museum, 567 pp. lan. Domning, D. P. Friant, M. 1978. Sirenian evolution in the North Pacific. 1963. Recherches sur la formule et la mor- Univ. California Publ. Geol. Sci. 118: phologie des dents temporaires des Chi- 1-178. ropteres. Acta Anat. 52: 90-101. Donoghue, M. J., J. A. Doyle, J. Gauthier, A. G. Fritsch, G. Kluge, and T. Rowe 1911. Contributions to the histology of the 1989. The importance of fossils in phylogeny Pteropus eye. Z. Zool. 98: 288. reconstruction. Annu. Rev. Ecol. Syst. Gauthier, J., A. G. Kluge, and T. Rowe. 20: 431-446. 1988. Amniote phylogeny and the importance Ducrocq, S., J.-J. Jaeger, and B. Sige of fossils. Cladistics 4: 105-209. 1993. Late Eocene southern Asian record of a Gopalakrishna, A. megabat and its inferences on the mega- 1958. Foetal membranes in some Indian Mi- bat phylogeny. Bat Res. News 33: 41- crochiroptera. J. Morphol. 102: 157- 42. [Dated 1992 but issued in 1993] 197. Duke-Endler, W. S. Gray, J. A., and A. J. Sokoloff 1958. System of ophthalmology, Volume 1, 1992. Propatagial innervation in the flying The eye in evolution. London: Henry squirrel Glaucomys volans. Am. Zool. Kimpton. 32: 157A. Ellsworth, A. H. F. Greenwald, N. S. 1974. Reassessment ofmuscle homologies and 1990. Cladistic analysis of chiropteran rela- nomenclature in conservative am- tionships: why megachiropterans are not niotes, the echidna, Tachyglossus, the primates. Bat Res. News 31: 79-80. opossum, Didelphis, and the tuatara, 1991. Primate-bat relationships and cladistic Sphenodon. Part 1: pelvic musculature. analysis of morphological data. Am. J. Huntington, NY: Robert E. Krieger. Phys. Anthropol., Supp. 12: 82. Enders, A. C., and W. A. Wimsatt Gregory, W. K. 1968. Formation and structure of the hemo- 1910. The orders ofmammals. Bull. Am. Mus. dichorial chorioallantoic placenta ofthe Nat. Hist. 27: 1-524. bat (Myotis lucifugus lucifugus). Am. J. Griffiths, T. A., and A. L. Smith Anat. 122: 453-490. 1991. Systematics of emballonuroid bats Felsenstein, J. (Chiroptera: Emballonuridae and Rhi- 1984. Distance methods for inferring phylog- nopomatidae), based on hyoid mor- enies: a justification. Evolution 38: 16- phology. Bull. Am. Mus. Nat. Hist. 206: 24. 62-83. Fischer, M. S. Griffiths, T. A., A. Truckenbrod, and P. J. Spon- 1989. Zur Ontogenese der Tympanalregion der holtz Procaviidae (Mammalia: Hyracoidea). 1992. Systematics ofmegadermatid bats (Chi- Gegenbaurs Morphol. Jahrb. 135: 795- roptera, Megadermatidae), based on hy- 840. oid morphology. Am. Mus. Novitates Fischer, M. S., and P. Tassy 3031: 21 pp. 1993. The interrelation between Proboscidea, Groves, C. P. Sirenia, Hyracoidea, and Mesaxonia: the 1993. Order Primates. In D. E. Wilson and D. morphological evidence. In F. S. Szalay, M. Reeder (eds.), Mammal species of 1994 SIMMONS: CHIROPTERAN MONOPHYLY 49

the world, a taxonomic and geographic contemporary mammals. Brain Behav. reference, 2nd ed., pp. 243-277. Wash- Evol. 20: 97-117. ington, DC: Smithsonian Institution Johnson, J. I., J. A. W. Kirsch, and R. C. Switzer Press. 1984. Phylogeny through brain traits: evolu- Habersetzer, J., and G. Storch tion of neural characters. Brain Behav. 1987. Klassifikation und funtionelle Fliugel- Evol. 24: 169-176. morphologie paliiogener Fledermiiuse Johnson, J. I., J. A. W. Kirsch, R. L. Reep, and (Mammalia, Chiroptera). Cour For- R. C. Switzer schungsinst. Senckenb. 91: 117-150. In press. Phylogeny through brain traits: more 1992. Cochlea size in extant Chiroptera and character for the analysis ofmammalian Middle Eocene microchiropterans from evolution. Brain Behav. Evol. Messel. Naturwissenschaften 79: 462- Jones, J. K., and H. H. Genoways 466. 1970. Chiropteran systematics. In R. H. Henson, 0. W. Slaughter and D. W. Walton (eds.), 1970. The central nervous system. In W. A. About bats: a chiropteran symposium, Wimsatt (ed.), Biology of bats 2: 57- pp. 3-21. Dallas, TX: Southern Meth- 152. New York: Academic Press. odist Univ. Press. Hill, J. E., and J. D. Smith Jones, T. R., A. G. Kluge, and A. J. Wolf 1984. Bats: a natural history. Austin, TX: 1993. When theories and methodologies clash: Univ. Texas Press. a phylogenetic reanalysis of the North Honeycutt, R. L., and R. M. Adkins American ambystomatid salamanders 1993. Higher level systematics of eutherian (Caudata: Ambystomatidae). Syst. Biol. mammals: an assessment of molecular 42: 92-102. characters and phylogenetic hypothe- Kaas, J. H. ses. Annu. Rev. Ecol. Syst. 24: 279-306. 1983. What, if anything, is SI? Organization Howell, A. B., and W. L. Straus of the first somatosensory area of the 1933. The muscular system. In C. G. Hartman cortex. Physiol. Rev. 63: 206-231. and W. L. Straus (eds.), Anatomy ofthe Kaas, J. H., and T. M. Preuss Rhesus monkey (Macaca mulatta), pp. 1993. Archontan affinities as reflected in the 89-175. New York: Hafner. visual system. In F. S. Szalay, M. J. No- Humphry, G. M. vacek, and M. C. McKenna (eds.), 1869. The myology of the limbs of Pteropus. Mammal phylogeny: placentals, pp. J. Anat. Physiol. 3: 294-319. 115-128. Berlin: Springer-Verlag. Hunt, R. M. Kallen, F. C. 1974. The auditory bulla in Carnivora: an an- 1977. The cardiovascular system. In W. A. atomical basis for reappraisal of carni- Wimsatt (ed.), Biology of bats 3: 289- vore evolution. J. Morphol. 143: 21-76. 483. New York: Academic Press. Jepsen, G. L. Kay, R. F., J. G. M. Thewissen, and A. D. Yoder 1966. Early Eocene bat from Wyoming. Sci- 1992. Cranial anatomy of Ignacius graybul- ence 154: 1333-1339. lianus and the affinities of the Plesiad- 1970. Bat origins and evolution. In W. A. apiformes. Am. J. Phys. Anthropol. 89: Wimsatt (ed.), Biology of bats 2: 1-64. 477-498. New York: Academic Press. Kellogg, R. Johnson, J. I., and J. A. W. Kirsch 1936. A review of the Archaeoceti. Carnegie 1993. Phylogeny through brain traits: inter- Inst. Washington Publ. 482: 1-366. ordinal relationships among mammals Kilpatrick, C. W., and P. E. Nunez including Primates and Chiroptera. In 1993. Monophyly ofbats inferred from DNA- R. D. E. MacPhee (ed.), Primates and DNA hybridization. Bat Res. News 33: their relatives in phylogenetic perspec- 62. [Dated 1992 but not issued until tive, pp. 293-331. Advances in prima- 1993] tology series. New York: Plenum Press. King, A. J. Johnson, J. I., J. A. W. Kirsch, and R. C. Switzer 1991. Re-examination ofthe basicranial anat- 1982a. Phylogeny through brain traits: fifteen omy ofthe Megachiroptera. Acta Anat. characters adumbrate mammalian ge- 140: 313-318. nealogy. Brain Behav. Evol. 20: 72-83. Kirsch, J. A. W. Johnson, J. I., R. C. Switzer, and J. A. W. Kirsch 1983. Phylogeny through brain traits: objec- 1982b. Phylogeny through brain traits: the dis- tives and method. Brain Behav. Evol. tribution of categorizing characters in 22: 53-59. 50 AMERICAN MUSEUM NOVITATES NO. 3103

Kirsch, J. A. W., and J. I. Johnson Zahnhomologien bei Chiroptera. Lunds 1983. Phylogeny through brain traits: trees Univ. Arsskrift. 14: 1-37. generated by neural characters. Brain 1886. Zur Anatomie der Beckenregion bei In- Behav. Evol. 22: 60-68. sectivora, mit besonderer Beriicksichti- Kirsch, J. A. W., J. I. Johnson, and R. C. Switzer gung ihrer morphologischen Beziehun- 1983. Phylogeny through brain traits: the ger zu derjenigen anderer Siiugethiere. mammalian family tree. Brain Behav. Kongl. Svenska Vetenskaps-Akade- Evol. 22: 70-74. miens Handlingar 20: 1-113. Klaauw, C. J. van der Le Gros Clark, W. E. 1922. Uber die Entwickelung des Entotym- 1924. The myology of the tree-shrew (Tupaia panicums. Tijdschr. Ned. Dierkd. Ver. minor). Proc. Zool. Soc. London 1924: 18: 135-174. 461-497. Kluge, A. G. 1926. On the anatomy of the pen-tailed tree- 1989. A concern for evidence and a phyloge- shrew (Ptilocercus lowii). Proc. Zool. Soc. netic hypothesis ofrelationships among London 1926: 1179-1309. Epicrates (Boidae, Serpentes). Syst. Zool. Luckett, W. P. 38: 7-25. 1975. Ontogeny of the fetal membranes and Knight, A., and D. P. Mindell placenta: their bearing on primate phy- 1993. Substitution bias, weighting ofDNA se- logeny. In W. P. Luckett and F. S. Szalay quence evolution, and the phylogenetic (eds.), Phylogeny of the primates, pp. position of Fea's viper. Syst. Biol. 42: 157-182. New York: Plenum Press. 18-31. 1977. Ontogeny of amniote fetal membranes Kolmer, W. and their application to phylogeny. In 1910. Contribution to the study of the eye of M. K. Hecht, P. C. Goody, and B. M. a macrochiropteran. Centralbl. Physiol. Hecht (eds.), Major patterns in verte- 23: 6. brate evolution, pp. 439-516. New 1911. The problem of the anatomy of the eye York: Plenum Press. of macrochiroptera. Z. Wiss. Zool. 97: 1980a. The suggested evolutionary relation- 91. ships and classification of tree shrews. 1926. On the eye of the bat. Verh. Zool. Bot. In W. P. Luckett (ed.), Comparative bi- Ges. Wien 74: 29-31. ology and evolutionary relationships of tree shrews, pp. 3-31. New York: Ple- Koopman, K. F. num Press. 1984. A synopsis of the families of bats, Part 1980b. The use of fetal membrane data in as- VII. Bat Res. News 25: 25-27. sessing chiropteran phylogeny. In D. E. 1993. Order Chiroptera. In D. E. Wilson and Wilson and A. L. Gardner (eds.), Pro- D. M. Reeder (eds.), Mammal species ceedings of the Fifth International Bat ofthe world, a taxonomic and geograph- Research Conference, pp. 245-265. ic reference, 2nd ed., pp. 137-241. Lubbock, TX: Texas Tech Press. Washington, DC: Smithsonian Institu- 1985. Supraordinal and intraordinal affinities tion Press. of rodents. In W. P. Luckett and J.-L. 1994. Order of bats; Chiroptera Blumenbach, Hartenberger (eds.), Evolutionary rela- 1779. Handbook of zoology 8(60): 1- tionships among rodents, pp. 227-276. 217. New York: Plenum Press. Koopman, K. F., and G. T. MacIntyre 1993. Developmental evidence from the fetal 1980. Phylogenetic analysis of chiropteran membranes for assessing archontan re- dentition. In D. E. Wilson and A. L. lationships. In R. D. E. MacPhee (ed.), Gardner (eds.), Proceedings ofthe Fifth Primates and their relatives in phylo- International Bat Research Conference, genetic perspective, pp. 149-186. Ad- pp. 279-288. Lubbock, TX: Texas Tech vances in primatology series. New York: Press. Plenum Press. Lapoint, F.-J., and G. Baron Luckett, W. P., and J.-L. Hartenberger 1993. Encephalization, adaptation and evo- 1993. Monophyly or polyphyly of the order lution ofbats: statistical evidence for the Rodentia: possible conflict between monophyly of Chiroptera. Bat Res. morphological and molecular interpre- News 33: 64. [Dated 1992 but issued in tations. J. Mammal. Evol. 1: 127-147. 1993] MacAlister, A. Leche, W. 1872. The myology ofthe cheiroptera. Philos. 1875. Zur Kenntniss des Milchgebisses und der Trans. R. Soc. London 162: 125-171. 1994 SIMMONS: CHIROPTERAN MONOPHYLY 51

MacPhee, R. D. E. controversies. In D. M. Hillis and C. 1981. Auditory regions of primates and eu- Moritz (eds.), Molecular systematics, pp. therian insectivores: morphology, on- 1-10. Sunderland, MA: Sinauer. togeny, and character analysis. Contrib. Mossman, H. W. Primatol. 18: 1-282. 1937. Comparative morphogenesis ofthe fetal MacPhee, R. D. E., and M. J. Novacek membranes and accessory uterine struc- 1993. Definition and relationships of Lipo- tures. Contrib. Embryol. Carnegie Inst. typhla. In F. S. Szalay, M. J. Novacek, Washington 26: 129-246. and M. C. McKenna (eds.), Mammal 1987. Vertebrate fetal membranes. New phylogeny: placentals, pp. 13-31. Ber- Brunswick, NJ: Rutgers Univ. Press. lin: Springer-Verlag. Novacek, M. J. MacPhee, R. D. E., M. J. Novacek, and G. Storch 1980a. Cranioskeletal features in tupaiids and 1988. Basicranial morphology of Early Terti- selected Eutheria as phylogenetic evi- ary erinaceomorphs and the origin of dence. In W. P. Luckett (ed.), Compar- Primates. Am. Mus. Novitates 2921: 42 ative biology and evolutionary relation- PP. ships of tree shrews, pp. 35-93. New Martin, R. D. York: Plenum Press. 1975. The bearing of reproductive behavior 1980b. Phylogenetic analysis ofthe chiropteran and ontogeny on strepsirhine phyloge- auditory region. In D. E. Wilson and A. ny. In W. P. Luckett and F. S. Szalay L. Gardner (eds.), Proceedings of the (eds.), Phylogeny of the primates, pp. Fifth International Bat Research Con- 265-297. New York: Plenum Press. ference, pp. 317-330. Lubbock, TX: 1990. Primate origins and evolution. London: Texas Tech Press. Chapman and Hall. 1985a. Evidence for echolocation in the oldest Matthew, W. D. known bats. Nature 315: 140-141. 1909. The Carnivora and Insectivora of the 1985b. Cranial evidence for rodent affinities. In Bridger Basin, Middle Eocene. Mem. W. P. Luckett and J.-L. Hartenberger Am. Mus. Nat. Hist. 9: 289-567. (eds.), Evolutionary relationships among Meschinelli, L. rodents, pp. 59-82. New York: Plenum 1903. Un nuovo chiroptero fossile (Archaeop- Press. teropus transiens Meschen.) delle liquiti 1986. The skull of leptictid insectivorans and di Monteviale. Atti Ist. Veneto Sci. Lett. the higher-level classification of euthe- Arti. Venezia Cl. Sci. Fis. Mat. Nat. 62: rian mammals. Bull. Am. Mus. Nat. 1329-1344. Hist. 183: 1-111. Miller, G. S. 1987. Auditory features and affinities of the 1907. The families and genera of bats. Bull. Eocene bats Icaronycteris and Palaeo- U.S. Nat. Mus. 57: 1-282. chiropteryx (Microchiroptera, incertae Mindell, D. P., C. W. Dick, and R. J. Baker sedis). Am. Mus. Novitates 2877: 18 pp. 1991. Phylogenetic relationships among 1990. Morphology, paleontology, and the megabats, microbats, and primates. higher clades of mammals. In H. Gen- Proc. Natl. Acad. Sci. USA 88: 10322- oways (ed.), Current mammalogy 2: 10326. 507-543. New York: Plenum Press. Miyamoto, M. M., and S. M. Boyle 1992a. Fossils, topologies, missing data, and the 1989. The potential importance of mitochon- higher level phylogeny of eutherian drial DNA sequence data to eutherian mammals. Syst. Biol. 41: 58-73. mammal phylogeny. In B. Fernholm, 1992b. Fossils as critical data for phylogeny. In K. Bremer, and H. Jornvall (eds.), The M. J. Novacek and Q. D. Wheeler (eds.), hierarchy oflife, Nobel Symposium 70, Extinction and phylogeny, pp. 46-88. pp. 437-452. Amsterdam: Excerpta New York: Columbia Univ. Press. Medica, Elsevier. 1994. Morphological and molecular inroads Miyamoto, M. M., and M. Goodman to phylogeny. In L. Grande and 0. 1986. Biomolecular systematics of eutherian Rieppel (eds.), Interpreting the hierar- mammals: phylogenetic patterns and chy of nature: from systematic patterns classification. Syst. Zool. 35: 230-240. to evolutionary process theories, pp. 85- Mori, M. 131. New York: Academic Press. 1960. Muskulatur des Pteropus edulis. Okaji- Novacek, M. J., and A. R. Wyss mas Folia Anat. Japonica 36: 253-307. 1986. Higher level relationships ofthe Recent Moritz, C., and D. M. Hillis eutherian orders: morphological evi- 1990. Molecular systematics: context and dence. Cladistics 2: 257-287. 52 AMERICAN MUSEUM NOVITATES NO. 3103

Novacek, M. J., A. R. Wyss, and M. C. McKenna 1992. Reproductivebiology ofthe female black 1988. The major groups of eutherian mam- mastiff bat, Molossus ater. In W. C. mals. In M. J. Benton (ed.), The phy- Hamlett (ed.), Reproductive biology of logeny and classification of the tetra- South American vertebrates, pp. 262- pods, pp.31-71. London: Oxford Univ. 282. New York: Springer-Verlag. Press (Clarendon). Reed, C. A. Nunez, P. E., and C. W. Kilpatrick 1951. Locomotion and appendicular anatomy In press. Monophyletic or diphyletic origin of in three soricoid insectivores. Am. Midl. bats as inferred by DNA-DNA hybrid- Nat. 45: 513-671. ization. Bat Res. News. Reinbach, W. Pedler, C., and T. Tilley 1952. Zur Entwicklung des Primordialcrani- 1969. The retina of a fruit bat. Vision Res. 9: ums von Dasypus novemcinctus Linne 909-922. (Tatusia novemcinctus Lesson) II. Z. Pettigrew, J. D. Morphol. Anthropol. 45: 1-72. 1986. Flying primates? Megabats have the ad- Revilliod, P. vanced pathway from eye to midbrain. 1922. Contribution a letude des chiropteres des Science 231: 1304-1306. terrains Tertiares 2. Mem. Soc. Paleon- 1991 a. Wings or brain? Convergent evolution tol. Suisse 45: 133-195. in the origins of bats. Syst. Zool. 40: Rouse, G. W., and S. K. Robson 199-216. 1986. An ultrastructural study ofmegachirop- 1991b. A fruitful, wrong hypothesis? Response teran (Mammalia: Chiroptera) sper- to Baker, Novacek, and Simmons. Syst. matozoa: implications for chiropteran Zool. 40: 231-239. phylogeny. J. Submicrosc. Cytol. 18: Pettigrew, J. D., and H. M. Cooper 137-152. 1986. Aerial primates: advanced visual path- Roux, G. H. ways in megabats and gliding lemurs. 1947. The cranial development of certain Soc. Neurosci. Abstr. 12: 1035. Ethiopian "insectivores" and its bear- Pettigrew, J. D., and B. G. M. Jamieson ing on the mutual affinities ofthe group. 1987. Are flying foxes (Chiroptera: Pteropod- Acta Zool., Stockholm 28: 165-397. idae) really primates? Aust. Mammal. Russell, D. E., and B. Sige 10: 119-124. 1970. Revision des chiropteres lutetien de Pettigrew, J. D., B. G. M. Jamieson, S. K. Robson, Messel (Hesse, Allemagne). Palaeover- L. S. Hall, K. I. McAnally, and H. M. Cooper tebrata 3: 83-182. 1989. Phylogenetic relations between micro- Sabeur, G., G. Macaya, F. Kadi, and G. Bernardi bats, megabats and primates (Mam- 1993. The isochore patterns of mammalian malia: Chiroptera and Primates). Phil- genomes and their phylogenetic impli- os. Trans. R. Soc. London B 325: 489- cations. J. Mol. Evol. 37: 93-108. 559. Sarich, V. M. Pierson, E. D. 1993. Mammalian systematics: twenty-five 1986. Molecular systematics of the Microchi- years among their albumins and trans- roptera: higher taxon relationships and ferrins. In F. S. Szalay, M. J. Novacek, biogeography. Ph.D. diss., Univ. Cali- and M. C. McKenna (eds.), Mammal fornia, Berkeley. phylogeny: placentals, pp. 103-114. Prothero, D. R., E. M. Manning, and M. Fischer Berlin: Springer-Verlag. 1988. The phylogeny of ungulates. In M. J. Scherer, S. Benton (ed.), The phylogeny and clas- 1990. The protein molecular clock: time for a sification ofthe tetrapods, vol. 2: mam- reevaluation. In M. K. Hecht, B. Wal- mals, pp. 201-234. Systematics Asso- lace, and R. J. Macintyre (eds.), Evo- ciation Special Volume No. 35B. lutionary biology 24: 83-106. New York: Oxford: Clarendon Press. Plenum Press. Rasweiler, J. J. Sig6, B. 1979. Early embryonic development and im- 1991. Morphologie dentaire lacteale d'un chi- plantation in bats. J. Reprod. Fertil. 56: roptere de 1' Eocene Inferieur-moyen 403-416. d'Europe. Geobios 13: 231-236. 1990. Implantation, development of the fetal Simmons, N. B. membranes, and placentation in the 1993. The importanc of methods: archontan captive black mastiffbat, Molossus ater. phylogeny and cladistic analysis ofmor- Am. J. Anat. 187: 109-136. phological data. In R. D. E. MacPhee 1994 SIMMONS: CHIROPTERAN MONOPHYLY 53

(ed.), Primates and their relatives in 1993. A molecular view of primate supraor- phylogenetic perspective, pp. 1-6 1. Ad- dinal relationships from the analysis of vances in primatology series. New York: both nucleotide and amino acid se- Plenum Press. quences. In R. D. E. MacPhee (ed.), Pri- Simmons, N. B., M. J. Novacek, and R. J. Baker mates and their relatives in phyloge- 1991. Approaches, methods, and the future of netic perspective, pp. 251-292. the chiropteran monophyly controver- Advances in primatology series. New sy: a reply to J. D. Pettigrew. Syst. Zool. York: Plenum Press. 40: 239-244. Stephens, R. J., and N. Easterbrook Simpson, G. G. 1968. Development of the cytoplasmic mem- 1945. The principles of classification and a branous organelle in the endodermal classification of mammals. Bull. Am. cells of the yolk sac ofthe bat Tadarida Mus. Nat. Hist. 85: 1-350. brasiliensis. J. Ultrastruct. Res. 24: 239- Slaughter, B. H. 248. 1970. Evolutionary trends ofchiropteran den- Stirckler, T. L. titions. In B. H. Slaughter and D. W. 1978. Functional osteology and myology ofthe Walton (eds.), About bats, pp. 51-83. shoulder in the Chiroptera. Contrib. Dallas, TX: Southern Methodist Univ. Vertebr. Evol. 4: 1-198. Press. Switzer, R. C., J. I. Johnson, and J. A. W. Kirsch Smith, J. D. 1980. Phylogeny through brain traits: the 1972. Systematics of the chiropteran family course ofthe dorsal lateral olfactory tract Mormoopidae. Misc. Publ. Univ. Kan- past the accessory olfactory formation sas Mus. Nat. Hist. 56: 1-132. as a palimpsest of mammalian descent. 1976. Chiropteran evolution. In R. J. Baker, Brain Behav. Evol. 17: 339-363. J. K. Jones, and D. C. Carter (eds.), Bi- Swofford, D. L. ology of bats of the new world family 1991. When are phylogeny estimates from Phyllostomatidae, Part I, pp. 49-69. molecular and morphological data in- Lubbock, TX: Spec. Publ. Texas Tech congruent? In M. M. Miyamoto and J. Univ. Cracraft (eds.), Phylogenetic analysis of 1980. Chiropteran phylogenetics: introduc- DNA sequences, pp. 295-333. New tion. In D. E. Wilson and A. L. Gardner York: Oxford Univ. Press. (eds.), Proceedings of the Fifth Inter- Szalay, F. S. national Bat Research Conference, pp. 1977. Phylogenetic relationships and a clas- 233-244. Lubbock, TX: Texas Tech sification ofeutherian Mammalia. In M. Press. K. Hecht, P. C. Goody, and B. M. Hecht Smith, J. D., and G. Madkour (eds.), Major patterns in vertebrate evo- 1980. Penial morphology and the question of lution, pp.315-374. New York: Plenum chiropteran phylogeny. In D. E. Wilson Press. and A. L. Gardner (eds.), Proceedings 1982. A new appraisal ofmarsupial phylogeny of the Fifth International Bat Research and classification. In M. Archer (ed.), Conference, pp. 347-265. Lubbock, TX: Carnivorous marsupials 2: 621-640. Texas Tech Press. Sydney: R. Soc. of New South Wales. Springer, M. S., and J. A. W. Kirsch 1984. Arboreality: is it homologous in meta- 1993. A molecular perspective on the phylog- therian and eutherian mammals? In M. eny ofplacental mammals based on mi- K. Hecht, B. Wallace, and G. T. Prance tochondrial 12S rDNA sequences, with (eds.), Evolutionary biology 18: 215- special reference to the problem of the 258. New York: Plenum Press. Paenungulata. J. Mammal. Evol. 1: 149- 1993. Pedal evolution ofmammals in the Me- 166. sozoic: tests for taxic relationships. In Stanhope, M. J., J. Czelusniak, J.-S. Si, J. Nick- F. S. Szalay, M. J. Novacek, and M. C. erson, and M. Goodman McKenna (eds.), Mammal phylogeny: 1992. A molecular perspective on mammali- Mesozoic differentiation, multituber- an evolution from the gene encoding in- culates, monotremes, early therians, and terphotoreceptor retinoid binding pro- marsupials, pp. 109-128. Berlin: tein. Mol. Phylog. Evol. 1: 148-160. Springer-Verlag. Stanhope, M. J., W. J. Bailey, J. Czelusniak, M. Szalay, F. S., and R. L. Decker Goodman, J.-S. Si, J. Nickerson, J. G. Sgouros, 1974. Origins, evolution, and function of the G. A. M. Singer, and T. K. Kleinschimidt tarsus in late Cretaceous eutherians and 54 AMERICAN MUSEUM NOVITATES NO. 3103

Paleocene Primates. In F. A. Jenkins Wible, J. R. (ed.), Primate locomotion, pp. 223-259. 1984. The ontogeny and phylogeny of the New York: Academic Press. mammalian cranial arterial system. Szalay, F. S., and G. Drawhorn Ph.D. diss., Duke Univ., Durham, NC, 1980. Evolution and diversification ofthe Ar- 705 pp. chonta in an arboreal milieu. In W. P. 1987. The eutherian stapedial artery: charac- Luckett (ed.), Comparative biology and ter analysis and implications for super- evolutionary relationships of tree ordinal relationships. Zool. J. Linn. Soc. shrews, pp. 133-169. New York: Ple- 91: 107-135. num Press. 1992. Further examination of the basicranial Szalay, F. S., and S. G. Lucas anatomy ofthe Megachiroptera: a reply 1993. Cranioskeletal morphology of archon- to A. J. King. Acta Anat. 143: 309-316. tans, and diagnoses of Chiroptera, Vol- 1993. Cranial circulation and relationships of itantia, and Archonta. In R. D. E. the colugo Cynocephalus (Dermoptera, MacPhee (ed.), Primates and their rel- Mammalia). Am. Mus. Novitates 3072: atives in phylogenetic perspective, pp. 27 pp. 187-226. Advances in primatology se- Wible, J. R., and H. H. Covert ries. New York: Plenum Press. 1987. Primates: cladistic diagnosis and rela- Thewissen, J. G. M., and S. K. Babcock tionships. J. Hum. Evol. 16: 1-22. 1991. Distinctive cranial and cervical inner- Wible, J. R., and J. R. Martin vation of ming muscles; new evidence 1993. Ontogeny ofthe tympanic floor and roof for bat monophyly. Science 251: 934- in archontans. In R. D. E. MacPhee, 936. Primates and their relatives in phylo- 1993. The implications of the propatagial genetic perspective, pp. 111-148. Ad- muscles of flying and gliding mammals vances in primatology series. New York: for archontan systematics. In R. D. E. Plenum Press. MacPhee (ed.), Primates and their rel- Wible, J. R., and M. J. Novacek atives in phylogenetic perspective, pp. 1988. Cranial evidence for the monophyletic 91-109. Advances in primatology se- origin ofbats. Am. Mus. Novitates 2911: ries. New York: Plenum Press. 1-19. Thiele, A., M. Vogelsang, and K.-P. Hoffman Wilson, D. E. 1991. Patterns ofretinotectal projection in the 1993. Order Scandentia. In D. E. Wilson and megachiropteran bat Rousettus aegyp- D. M. Reeder (eds.), Mammal species tiacus. J. Comp. Neurol. 314: 671-683. ofthe world, a taxonomic and geograph- Van Valen, L. ic reference, 2nd ed., pp. 131-134. 1979. The evolution of bats. Evol. Theory 4: Washington, DC: Smithsonian Institu- 104-121. tion Press. Vaughan, T. A. Wise, L. Z., J. D. Pettigrew, and M. B. Calford 1959. Functional morphology of three bats: 1986. Somatosensory cortical representation Eumops, Myotis, Macrotus. Univ. Kan- in the Australian ghost bat, Macroder- sas Publ. Mus. Nat. Hist. 12: 1-153. ma gigas. J. Comp. Neurol. 248: 257- 1970a. The skeletal system. In W. A. Wimsatt 262. (ed.), Biology of bats 1: 97-138. New Wyss, A. R., and J. J. Flynn York: Academic Press. 1993. A phylogenetic analysis and definition 1970b. The muscular system. In W. A. Wimsatt of Carnivora. In F. S. Szalay, M. J. No- (ed.), Biology of bats 1: 139-194. New vacek, and M. C. McKenna (eds.), York: Academic Press. Mammal phylogeny: placentals, pp. 32- Walton, D. W., and G. M. Walton 52. Berlin: Springer-Verlag. 1970. Post-cranial osteology of bats. In B. H. Zeller, U. A. Slaughter and D. W. Walton (eds.), 1986. Ontogeny and cranial morphology ofthe About bats: a chiropteran biology sym- tympanic region of the Tupaiidae, with posium, pp. 93-126. Dallas, TX: special reference to Ptilocercus. Folia Southern Methodist Univ. Press. Primatol. 47: 61-80. Wheeler, W. Zook, J. M., and B. C. Fowler In press. Sequence alignment, parameter sen- 1982. Central representation of a specialized sitivity, and the phylogenetic analysis of mechanosensory array in the wing of a molecular data. Syst. Biol. bat. Soc. Neurosci. Abstr. 8: 38.

Recent issues of the Novitates may be purchased from the Museum. Lists of back issues of the Novitates, Bulletin, and Anthropological Papers published during the last five years are available free of charge. Address orders to: American Museum of Natural History Library, Department D, Central Park West at 79th St., New York, N.Y. 10024.

E This paper meets the requirements of ANSI/NISO Z39.48-1992 (Permanence of Paper).