Pp. 27-42, In Bat Biology and Conservation (T.H. Kunz and P.A. Racey, eds.). 1998. Smithsonian Institution Press, Washington. - 2 In the Minotaur's Labyrinth Phylogeny of the Bat Family Hipposideridae WIESLAW BOGDANOWICZ AND ROBERT D. OWEN

The family Hipposideridae is composed of nine Recent view or have made only minor changes to his 1963 dassi- genera with about 65 species, which are widespread fication. However, the question arises as to what extent throughout warm areas of the Old World from western Hill's carefully arranged, but nevertheless intuitive, species Africa east to the New Hebrides hdextend only marginally groups reflect phylogenetic history into the Palaearaic (Corbet and Hill 1991, 1992; Koopman More importantly, none of the previous studies evalu- 1994). The genus Hipposideros has about 50 speaes; the ated phylogenetic affinities within the entire family The other genera either are monotypic (Anthops, Cloeotis, Para- aim of our chapter is to fill this gap, although the lack of coelops, Rhinonycteris) or have 2 species (Aselliu, Asellism, well-preserved materials for some taxa makes our analysis Coelops, Triaenops). Hipposiderid fossils are known from the incomplete. Nevertheless, it is a first step toward a compre- middle Eocene of Europe (Sigk and Legendre 1983; Sigk hensive revision of phylogenetic relationships among hip- 1991), the early Oligocene of Arabo-Africa (Sigk et al. 1994), posiderids. We also evaluated different hypotheses concern- the late Oligocene of Australia (Archer et al. 1994), and ing the geographic center of origin for the family and the probably the Miocene of Asia (K. E Koopman, in litt.). monophyly of the genus Hipposideros. These assessments During the past 150 years hipposiderids have a&aaed were made through phylogenetic analyses of metrical and the attention of numerous taxonomists (summarized by discrete-state characters of the cranium, dentition, and ex- Hill 1963). The most prominent studies in this century were ternal morphology. those by Tate (1941) and Hill (1963) of the genus Hip- posideros and by Hill (1982) of the genera Rhinonycteris, Cloeotis, and Triuenops. Their work resulted in recognition Materials and Methods of 11 (Tate 1941) or 6 (Hill 1963) supraspecific groups Speaes, Specimens, and Measurements .,within the genus Hipposideros. Most of the more recent researchers (e.g., Jenkins and Hill 1981; KO& and Bhat Our study was based on 57 species and 702 adult specimens 1994; Koopman 1994) either have accepted Hill's point of (skins and skulls), each of which had no or few missing char- Table 2.1 Common-Part-Removed Analysis

n n Species (sexed + unsexed) RZ Speaes (seared + unsexed)

Antkops omatus Hipposideros incxpeMtrcJ Asellia patrizii Hipposiderosjonesi Aseuia hidm Hipposidnos Lankadiva krrchstoliczknnw Hipposideros Lawatus Ascuisncc hicllspidatrcc Hipposideros lrkaguli Clowris ptnivali Hipposidcros lyki Coelopsfritki Hipposidrms macrobullatus Cocbps robitrconi Hipposideros magktaylorac Hipposidms abae Hipposidcros marisae Hipposidnos annigcr Hipposideros magaloris Hipposidcros ater Hipposideros mwcinw Hipposidms beam Hipposideros obsm Hipposidms bicolor Hipposidcros papa Hipposideros Hipposideros pomona Hipposidcros calcaratus Hipposideros pratri Hipposidcros camm- Hipposideros pygmaem Hipposidms cnvinw Hipposideros ndlryl Hipposidms cineraceus Hipposideros nrbcr Hipposidcros commcrsoni Hipposideros sabanw Hipposideros cotynophyUw Hipposidnos smi Hipposidnos curhis Hipposideros speorir Hipposideros cydops Hipposideros srotoris Hipposidcros diadonn Hipposideros tcrluotric Hipposideros dinops Hipposideros hcrpis Hipposidms dyacmm Hipposideros wollastoni Hipposidcrosfiliginosus Rhinonyctnic aurantius Hipposidcrosfitlw TriMIopsfitdw Hipposidcros galmjhu Ttiaolops pmicus Hipposidcros haloplryllw

Notu: This cable h ingroup nra (Hipposiduidae),number of specimens (n), and coc5cient-of-determination(~3 values adjusted for degrees of fieedom hmlinear reps- sion of each ingroup taxon on a multiple-member outgroup (Rhinolophur ccIrW, n = 12; R. divosus, n = 10; R. hipporidnw, n = 12; R,malayanus, n = 8; andR, sin- n = 9). When multiplied by 100, R' indicates percentage of original vaxiance explained by the outgroup

acters (Table 2.1). Adults were recognized by fused epiphy- included the claws. Other measurements followed Freeman ses in wing bones. Hipposideros schistaceus was found to be (1981). Rautenbach (1986), and Bogdanowicz (1992). Fore- morphologically very similar to or even indistinguishable arm lengths given in Results are from Koopman (1994). I from H. Zankadiva (I? J. J. Bates, personal communication;our 1 observations); consequently, it was not treated as a distinct Transformations species. Space limitation precludes a list of specimens exam- ined, but this list is available on request fiom the first author All continuous values were transformed to their natural via Internet at [email protected]. logarithms, and the value of each characterwas calculated as A total of 45 cranial, dental, and external characters were the average of the means for males and females. Where measured with a Sylvac electronic caliper directly con- possible, samples fiom single or neighboring populations nected to a PC-compatible laptop computer for automatic were used for each speaes. For two endemic speaes without data capture. The width and helght of the foramen mag- evident sexual dimorphism (Anthops ornatus and Triaenops num (not included in Table 2.2) were used to calculate the firculus), unsexed specimens also were used. - foramen magnum area according to the formula given by The common-part-removedtransformation (Wood 1983) -Itadinsky (1967). Measurements were taken to the nearest was applied to remove the portion of variance accounted 0.01 rnm for cranial and dental characters and to the nearest for by regression onto selected rhinolophid taxa. Because 0.1 mm for external characters. The length of the hindfoot Rhinolophidae is the sister-taxon to the Hipposideridae Table 2.2 - Size-Out Analysis

Character PC1 PC2 PC3 PC4

Greatest skull length Condylocanine lengrh Least interorbiral breadth Zygomatic breadth Mastoid breadth Breadth of braincase Breadth of nasal swellings Height of braincase (excluding bullae) Length of maxillary toothrow Length of upper molarifonn row Width across upper canines Height of upper canine Width across upper third molars Length of upper third molar Width of upper third molar Supraorbital length Palatal length Area df foramen magnum Bullar length Bullar width Greatest lengrh of mandible Length of mandiiular toothrow Postdental length Helght of mandibular ramus Height of lower canine Coroaoi&angular distance Length of moment arm of temporal Length of moment arm of masetter Forearm length Third digit, metacarpal length Third digir, first phalanx length Third digit, second phalanx length Fourth digit, metacarpal lengrh Fourth digit, first phalanx length Fourth ckgit, second phalanx length Fifth digit, metacarpal length Fifth digit, first phalanx length Fifch digit, second phklength Head and body length Tail length Ear length Tibia length Hindfoot length Greatest breadth of anrerior noseleaf Greaten breadth of horseshoe (including secondary leaflets)

AU characters, variance explained (89.9%) (3.1%) (1.5%) (1.1'70)

Note: Data are character loadings for the first four prinapal components (PC)-aud, in parcnthucr at the end of the table, the percentages of variance they qlain-hm prinapal-componentsanalysis of the comlarion matrix. Analysis was based on 57 tan of the Hipposideridae and the average of 6vc speaes of Rhinobpkus @ cekM, R climnct, R, hipporidnos, R mn+us, and R. rink). (e.g., Novacek 1991), this regression function provided an sists of d groups that occur more than 50% of the time estimate of ancestral hipposiderid morphology In this' (CONSENSE program of PHYLIP;Pelsenstein 1993). study, the vector of character values for each hipposiderid species was regressed separately onto the means of those PARSIMONY ANALYSIS. The analysis was based on a set of as. for Rhinolophw celebensis, R. clivosus, R. hipposideros,R. malay- many as 30 possibly discrete-state cranial, dental, and exter- anus, and R. sinicus. For each ingroup taxon, the vector of nal characters (Appendix 2. I), scored from each adult speci- residuals was retained. These vectors were combined and men. The ingroup included 57 species and eight of the nine used in further calculations in the form of a transformed extant genera of the Hipposideridae. Multiple outgroup data matrix. taxa were used to polarize the character states, enhancing Another method used was a "size-out" procedure. Afier the prospect of correctly identifying autapomorphic fea- averaging the log-transformed values, a correlation matrix tures in the outgroup. The characters for analysis were was calculated and a principal component analysis was per- selected after their extensive evaluation fiom'a large series formed on the matrix. From this, the mauix of projections of specimens. The outgroup was composed of the sister- of each speaes of each component was calculated. The first family Rhinolophidae, represented by Rhinolophus celebemis, principal component, which primarily reflected sue rela- R. coelophyllus, R. hipposideros, R. luctus, R. malayanus, and tionships, was then deleted from the matrix, and the remain- R. sinicus. Megadermatidae (Cardiodenna cor, Megaderrna ing prinapal component scores were taken to be charaaer- Zyra, and M. spasma) and Nycteridae (Nycteris hispida, N. gran- state values for a newly created suite of characters. The dis, and N. tkbaica) were used as further outgroup taxa. The - foregoing calculations were made using the multiple linear Rhinopomatidae (Rhinopoma microphyUum) completed the regression analysis and factor analysis procedures from the outgroup (see Novacek 1991). A hypothetical ancestor of SPSS for Windows package (NaruMs 1993). the Hipposideridae was designated, and all character s~~~s were polarized by the outgroup comparison method of Maddison et al. (1984). Phylogenetic Analyses Cladograms were constructed using the branch-and- bound algorithm (Hendy and Penny 1982), with the option MAXIMUM-LIKELIHOODMETHOD. The common-part-removed for reconsidering an order of speaes that is included in and size-out data matrices were subjected to the CONTML, PHYLIP version 3.5 under UNIX (Felsenstein 1993).As many procedure of PHYLIP (Felsenstein 1993), which estimates as 3 1,286 most-parsimonious trees were obtained during a phylogenies by the restricted maximum-likelihood method single run for lo,ooo,ooo possible trees. To compare trees based on the Brownian motion model. This algorithm, and define areas of congruence, we again used the majority. used primarily for genetic distance data, makes four as- rule consensus procedure. In a final consensus tree, however, sumptions concerning the data: (1) the lineages evolve inde- we also indudedgroups that occur less than 50% of the time, . pendently; (2) after lineages separate, their genetic (and working downward in their frequency of occurrence, so morphometric) evolution proceeds independently; (3) drifi, long as they continue to resolve the tree and do not contra- rather than selection, is the cause of evolutionary change; dict more frequent groups (CONSENSE program of and (4) each character drifts independently. These assurnp- PHYLIP; Felsenstein 1993). In this respect, the method is tions, although never met absolutely in our study (or prob- similar to the Nelson consensus method (Nelson 1979) al- ably in any phylogenetic study), have been discussed more though not identical (Felsenstein 1993).Tree lengths, consis- thoroughly by Felsenstein (1981) and by Bogdanowicz and tency and retention indices were calculated by Hennig86 Owen (1992). In each case, we used global optimization in version 1.5, using the mhennig* and bb* options (Farris 1988). search for the best tree, which resulted in about 15,000 tree These parameters may have been slightly underestimated topologies being compared each time. For both analyses. because of an overflow of the available tree space in the Rhinolophus celebemis, R. clivosus, R. hipposideros, R. malay- software used. anus, and R. sinicus were included to provide a root for the tree (Nwacek 1991). In the common-part-removed data, Morphological Dispersion Rhinolophus spp. were represented by a vector of zeros (Bogdanowicz and Owen 1992). Because results are de- Morphological clqersion of the fauna may be determined pendent on the order in which the speaes are encountered by calculating each taxon's aGrage phenetic distance fiom - in the data set, each analysis was repeated 50 times with every other taxon in the fauna, summing the averages, and different orderings of the input taxa. To compare trees and computing the faunal average (Findley 1976; Freeman 1981; define areas of congruence, we used the majority-rule con- Bogdanowicz 1992). In our studies, the average taxonomic sensus procedure. The majority-rule consensus tree con- distances (NTSYS-pc package; Rohlf 1993) between every Phylogeny of the Hipposim 31.

pair of speaes in a fauna were computed based on a matrix that the portion of the vector variance accounted for by the of standardized residuals. The Kruskall-Wallis nonpara- outgroup ranged from 79.6% (Coelops robinsoni) to 99.4% . metric test was used to evaluate digerences among average (Hipposiderosgaleritus) (see Table 2.1). Thus, the maximum-

faunal values. Because no nonparametric multiple-range , likelihood analyses were performed on residuals vectors; test exists for unequd sample sizes, the Mann-Whimey representingfiom 20.4% to 0.6% of the originalvariance in

U-test was conducted on all pairwise combinations of four ' the data from each speaes. faunas (nonparametric tests procedure of the SPSS pack- The majority consensus tree, computed from 50 original age; NaruSis 1993). Geographic affiliations of hipposiderid dadograms that were produced by changing the order of groups were based on Wallace's zoogeographic divisions input taxa, indicates the existence of six relatively stable (Lincoln et al. 1982). groups within the family (Figure 2.1): two of these are monotypic, two are characterized by 34speaes, and two comprise as many as 24-25 taxa. The monotypic groups are Results composed of the Philippine species Hipposideros pygmaeus and the Australasian Aselliscus.hiclcs;pidatus.Within the mul- Common-Part-Removed Analysis tispecies dusters, the first one contains four small taxa Multiple linear regressions of character vectors of each length, <50 mm) from the genus Hipposideros* on ,.hat of the outgroup (~hi~~l~~hi,-~~~)revealed which are limited in their present distribution to New

Figure 2.1. Majority consensus dadogram.&om stenqtis ' C 50 maximum-likelihood analyses of cornmon- musclnus C semonz C part-removed continuous-statedata. Stars mark wollastoni k the taxonomic groupings that appear in 95% or pygmaeus B more of the uees. Lectws that follow raxon dyacorum B C. percivali names denote speaes-groupmembershy, A. s toliczkanus according to W (1963) and Koopman (1994): A, sabanus B annigcr; B, bicolor; C, cyclops; D, diadnna; M, cal caratus B P, bicolor B megalotic; pratti; S, .yeoris. fulvus B clneraceus B j'onesi B ri dleyi B marlsae B curtus B megalotis M -macrobulla tus B B ha1 ophyll us B B bea tus B B S fuliginosus B sweoris S I 3CC g;ileri tus B cervinus B obscurus A. tridens A. patrizii lylei 1ekaguli pratti . armlger H terasensis - A

- A. ornatus - 3CC camerunensis C cyclops C I ' commersoni D 1arva t us S papua B maggietaylorae B- A. tricuspidatus R. aurantius T. persicus T. furculus Guinea or northern Australia. The next two assemblages Size-Free Analysis are formed by both Hipposideros and non-Hipposideros spe- aes from different regions of the Old World. Interestingly, The first principal component of log-transformed mor- all Hipposideros occurring in the first of these assemblages phometric data explains 89.8% of the variation, and all are characterized by small or medium forearm lengths, characters have high positive loadings on this component 3- which frequently are less than 50 mm and almost never (see Table 2.2). The second through fourth components exceed 66 mm (H. fiIiginosus, 56-64 mm; H. abae, 55-66 explain 3.1%, 1.5%, .and 1.1%, respectively; each of the -. mm). The second assemblage is dominated by large and remaining components account for less than 1.0% of the medium bats such as H. pratti (forearm length, 81-89 rnrn), variance. After removal of the first-component projections, . . H. inexpectaty (100-101 mm), H. dinok(93-97 mm), and H. the maximum-likelihood analysis was conducted on vectors commersoni (77-1 15 mm). The only exception is the small H. from the remaining 44 components. obscurus (40-52 mm) &om the Philippines. The last The majority consensus tree based on 50 size-free cla- polytypic duster is formed by the Australian species Rhi- dograrns indicates very few groups that maintain stable . nonycteris aurantiw, the Malagasy Ttiaenopsfirculw, and the structure under reordering of taxa in the data set (Figure primarily African T persicus, All three taxa have similar 2.2). A few groups contain pairs of species morphologically . noseleaf structure and geitly expanded zygoma. similar to each other (e.g., H. camerunensis and H. cyclops;

Figure 2.2. Majority consensus dadogram hm 50 maximum-likelihoodanalyses of size-fiee I ri dl eyi B continuouskate data. Stan mark the taxonomic stenotis C halophyl lus B groupings that appear in 95% or mon of the camerunensis C trees. Letters that follow taxon &es denote cvclons-a C --- speaes-groupmembership according to Hill C. roi;insoni . - *, macrobullatus B (1963) and Kooprnan (1994): A, anniger; B, bicolot: lylei P C, cyclops; D, diadm; M, megalotic; P, pratti; S, pomona B ater B spcwic. -- ruber -B muscinus C speor~s S maggietaylorae B abae S dyacorum B R. aurantius T. furculus inexpectatus D wollastoni C f ul iginosus B beat us B di adema I) obscurus B corynophy~lus C conunersonl D C. percivali A. ornatus larvatus S A. patrizii 1ankadiva D sabanus B bicol or B fulvus B axmiger A terasensis A marisae B A. tridens C. frithi cineraceus B 3CI galeri tus B cervlnus B pygma eus B pratti P curtus B )ones1 B megalotis M 3C- 3C- dinops D A. s to1iczkanus cal caratus B papua B i T. persicus A. tricuspida tus semoni C 1ekaguli D Phylogeny of the HipposiAeriAae 33 and H. gabitus and H. cervinm). The majority however, particular tree topology. This determination is reflected in show no dear connections, even in the case of dusters with the relative stability of several dades present in the majority the 95% repeatability of branches (e.g., H. rnacrobullutus and consensus tree, albeit this stability was exhibited mainly at H. lylei; and H.dinops and A. stoliczkanus). the top of the tree. The affinities of the basal dades are less likely to be consistent, and it seems that at least four species Parsimony Analysis of could be treated as basal taxa: Hipposideros bicolot; H.fitlws, Discrete-State Characters H. sernoni, and H. muscinus (Figure 2.3). These hipposiderids differ from their hypothetical ancestor in that the center of The branch-and-bound algorithm gave 3 1,286 most-parsi- the posterior border of hard palate is anterior to the poste- monious trees with length of 99, consistency index of 0.32, rior curvature of the palate bone (character 9) or is spicu- and retention index of 0;69. In general, a low consistency lated (character 10) (but see H. mmcinw), and that metacar- index indicates that the data matrix does not "fit". the tree pal N is longer than metacarpal V (character 29) (Appendix well (i.e., contains much homoplasy). A fairly good reten- 2.2). In fact, the latter character is a synapoinorphic feature tion index value suggests, however, that many of the char- of all the taxa studied, although it has been reversed in the acters used are only partly homoplasious and that their two Coelops species and H. corynophyllus. transformation series show some synapomorphy for the Above the four basal taxa, a trichotomy is formed from

Figure 2.3. Nelson-like consensus dadogram megalotis M &om parsimony analysis of disarte-statedata. cineraceus B pomona B Numbers at the forks indicate the pucentage of sabqus B times that the group consisting of the species marzsae B which ax to the right of that fork occurred ri dl eyi B halophyllus among the 31,286 trees. Lena that follow taxon macrobullatus 'g names denote spetiu-groupmembership ater B according to Hill (1963) and Koopman (1994): A, C. robinsoni C. friei armign: B, bicolq C, cyclops; D,diadem; M, C. perclvali megabtir; P, pratti; S, sped. pygmaeus B R. aurantius A. tricus~idatus A. stoliczkanus curtus B jonesi B T. furculus T. persicus A. ornatus A. tridens A. patrizji connnersonl D lankadiva D dinops D diadema D inexpectatus D annlger A tuzpls A pra t ti P speoris S f ul iginosus B obscuz-us B -wa~ua - B larvatus S co~ynophyllus C lyl ei P tsrasensis A stenotis C cyclops C wollastoni C 1ekagul i D camerunensis C bea tus B ruber B abae S dyacorum B gale+ tus B cervlnus B caff er B cal cara tus B maggGetay1 orae ,, B musc1nus C semonl C bicol or B fulvus B' 34 W BOGDANOWICZ AND R. D. OWEN

Rhinolophidae Hipposideridae ~ustralianregion

Oriental region

Palaearct region

/. 3 Ethiopian region 6 6 4 x = 1.01 4 2 2 Figure 2.4. Distribution of average distances among rhinolophid faunas (Bogda- 0 O nowicz 1992) and hipposiderid faunas (this study) 0.5 1.0 1.5 2.0 2.5 0.5 1.0 1.5 2.0 2.5 infourzoogeographicfegions.5 = overall mean Average taxonomic distance taxonomic distance. three polytypic lineages, one of which (upper lineage in relationships are not stable and several different tree topolo- Figure 2.3) can be found in all original trees. This dade gies may exist (see Figure 2.3). comprises nine fairly small Asian and African species (fore- arm length, 548 mm), including large-eared H. megalotis Morphological Dispersion and Origin &om Kenya and Ethiopia. These species are dosely related of the Hipposideridae chiefly because they have one or both of the following features: a cranium that is relatively broad across the mas- For hipposiderids fiom the Ethiopian, Palaearctic, Oriental, toids (character 4) and a foramen ovale of medium size and Australian regions, the average taxonomic distance val- (character 11). Both characters are partly homoplasious, ues range fiom 1.02 to 1.07 (Figure 2.4) and the differences and the latter especially shows strong parallelism with the among the four faunas are not statistically si@cant second lineage (largest, central lineage), grouping all the (Kruskall-Wallis H-test., a = 0.05). Painvise comparisons remaining dades that are common to all competing trees. also indicate that none of the.studied faunas is more dis- The other characteristic feature of this lineage is the pres- persed than another, although a nearly significant differ- ence of both Hipposideros and non-Hipposideros taxa and ence was observed between the Palaearctic and Australian sister-group relationships of large hipposiderid bats (e.g., H. faunas (Mann-Whitney U-test, p = 0.051), with the Palae- commersoni, H.lankadiva, H. dinops, and H. inexpectatus) and arctic fauna being more dispersed morphologically genera other than Hipposideros. Within the third lineage, In contrast, the distribution of average values isdifferent Pkylogeny of the Hipposideridae. 35

in different faunas. The Ethiopian and Australian regions taxa in the analysis, are only slightly less than the expected are characterized by values more or less symmetrically dis- value (0.32 versus 0.34). Missing data, however, may also tributed (skewness, '0.25 and 0.97, respectively), whereas mask the presence of homoplasy and give higher consis- those distributions in the Oriental and Palaearaic regions tency index values for matrices, with many cells scored as are skewed to the right (skewness, 1.52 and 1.88, respec- I"(Sanderson and Donoghue 1989). tively). These results suggest that the Oriental and Palae- Despite these possible limitations, the consensus da- '. , arctic faunas are composed of a majority of speaes that dograms derived from the common-part-removed and morphologically are dose to their nearest neighbor. The discrete-state matrices have several features in common. most distinctive species is Coelops robinsotti (average taxo- First, both confirm dose phylogenetic relationships be: nomic distance, 1-41)from the Oriental region, which to- tween members of the diaderna and armiger groups (Hill gether with C. fnthi can easily be identified by the presence 1963). Second, the three species from the speoris group are of a mdirnentary tail and unusually short ears. much like certain species from the bicolor group. In our opinion, the taxonomic status of both groups needs to be redefined and revised.(see also Kock and Bhat 1994). Third, Discussion large-eared H. (Syndemotis) megalotis of the megalotis group, Phylogenetic Relationships among Hipposiderids which is believed to be a single living descendant of the and Monophyly of the Genus Hipposderos middle Miocene Syndesmoris lineage (Legendre 1982), con- stitutes a dade together with some bats of the bicolw group For the two metrical data sets used in this study, the transfor- (see Figures 2.1 and 2.3) belonging to the subgenus Hip- mation to remove the commonpart resultedin simcantly posideros. Such a phylogenetic position of H. megalotis con- higher stability of dades than did the transformadon to tradicts both its subgeneric and its supraspedfic grou.P va- remove size. The relationships suggested by the comrnon- lidity (see Hill 1963; Legendre 1982). Fourth, primarily part-removed dadogram were more or less in good agree- ficanAsellia species and Southeast Asian Coelops species, ment with Hill's (1963) arrangements of Hipposideros taxa, as well as Anthops ornatw fiom the Solomon Islands, consis- grouping the majority of bats from the bicolor group into tently occur within the dades compoSed of the Hipposideros one dade and those from diaderna, pratti, and amiger into taxa. In our opinion, this suggests that the genus Hip- the other (see Figure 2.1). This was not the case with the posideros does not comprise all the descendants of an ances- size-free majority consensus tree (see Figure 24, where tor and most probably should be treated as a paraphyletic even the dades with the highest repeatability frequently group. contained taxa without dear phylogenetic connections. On the basis of fossil evidence, Legendre (1982) noted Interestingly, evolutionary affinities within the sister- that species of the &ct subgenus Hipposideros (Pseudorhi- family Rhinolophidae were also better explained by the nolophus) are morphologically similar to some large Recent common-part-removed dadogram than by the size-he taxa, such as H. amiger, H. diaderna, and H. commersoni, and dadogram (Bogdanowicz and Owen 1992). Wood (1983) could be ancestral to Asellia (see also Sigk 1968). Both con- reached similar conclusions, although about phenetic rela- sensus dadograms (see Figures 2.1 and 2.3) may support tionships, in his studies of storks (Ciconiidae) and cranes this hypothesis. (Gruidae). In combination, these studies suggested that the The status of the other non-Hipposideros genera seems to use of the common-part-removedmethod may be applica- be more complicated. Rhinonycteris aurantiw is thought to ble to the phylogenetic dassifications of at least those ver- be closely related to Brachipposideros nooraleebus from the tebrates, such as bats and birds, that exhibit determinate middle Miocene deposits from Riversleigh, Australia (Sigk growth. et d. 1982; Hand 1993; Archer et al. 1994). The common- The discrete-state consensus dadogram (see Figufe 2.3) part-removed and discrete-state dadograms do not conks- did not corroborate current systematic arrangements, and dict this interpretation, although the position of Rhino- several taxa traditionally thought to be dose systematically, nycteris in the second of these cladograms may indicate its such as those fiom the bicolor group, occurred in Merent doser relationships with large rather than small Hippo- dades; this may have resulted from a lack of sufticient sideros speaes. In the light of the microcomplement fixa- material. A low character-to-taxon ratio (30:57) and the tion transferrin data, however, Rhinonycteris is outside both absence of some data (see Appendix 2.2) reduce the support the Hipposideros and Rhinolophus genera (Pierson 1986). Its for dades that include relatively incomplete taxa. On the distance fiom these genera (103 and 110 units, respectively) -other hand, the obtained consistency index values of origi- was substaritially greater than the distance between them hal most-parsimonious trees, given the large number of (74 and 84 units). AseZZisncr was much doser (44 versus 81 units) to Rhinolophus than to Hipposideros, and about the wider than it is today (Hand 1984; Sevilla 1990). Their oldest same distance from Hipposideros as was Rhinolophus (81 and remains are known from the late middle Eocene of Europe

I 84 units, respectively). Evidently the results of morphologi- (e.g., Sigk and Legendre 1983; Sigk 1991). ~asedon fossil cal and immunological data may not be comparable at all evidence, hipposiderids were present in Arabo-Africa and levels in the phylogeny Optimum resolution at different Australia by the early and late Oligocene (Archer et al. 1994; evolutionary levels by albumin, electrophoretic, chromoso- Sigk et al. 1994), respectively In contrast, their known fossil

mal, and morphological characters was shown by Arnold et remains in the Oriental region are very few and relatively ' '

al. (1982) in a study on phyllostomoid bats. young, dating back only to the Neogene (Hand 1984, p. 883; , K. E Koopman, in litt.). In our opinion, however, the lack of Morphological Dispersion, Cladograms, older Oriental material should provisionally be treated as an and Center of Origin artifactual product of the general unavailability of well-ex- ' amined fossil material from this region, because we find Findley (1976) reasoned that older bat faunas are pheno- support from the neontological data to indicate that the typically more diverse. Our analysis indicated that, unlike Hipposideridae, like their sister-family Rhinolophidae (Bog- rhinolophids (Bogdanowicz and Owen 1992), hipposiderids danowicz and Owen 1992), most probably originated in have no significant differences in morphological dspersion Asia, not in Afiica (but see SigC 1991). This hypothesis of among the Ethiopian, Palaearctic, Oriental, and Australian origin would also be consistent with the paleodimatic evi- regions (see Figure 2.4). Our results suggest (albeit weakly) dence of tropical rainforest development in Southeast Asia that the Palaearctic fauna might be older than the Austra- during the Tertiary (Heaney 1991), as it is generally agreed lian fauna (Mann-Whimey U-test, p = 0.051), and this hy- that the family Hipposideridae would have developed and pothesis, while considering the age of fossil taxa, agrees radiated in such conditions (B. Sig6, in litt.). with palaeontological findings. ct The maximum-likelihood dadograms do not give any Karyology and Phylogenetic Relationships constructive suggestion about the center of origin for the family because at least six dades might be ancestral (see As far as we are aware, karyotypes of 22 hipposiderid spe- Figures 2.1 and 2.2). On the other hand, the most basal cies have been described (Table 2.3);"si.x diploid chromo- hipposiderids on the consensus dadogram derived from the some numbers have been encountered for these speaes, discrete-state data (Figure 2.3) are recently known from with only two within the genus Hipposideros (2n = 32, 52). Afghanistan, Pakistan, India, and Sri Lanka (H.fUlm), and It is very important for phylogenetic considerations to from Thailand, Malaysia, Indonesia, and the Philippines (H. determine the mode and direction of karyotypic change in bicolor). The next two basal species (H. smiand H. mu- the family studied. First, at the level of nondifferentially cinus) are limited in their present distribution to New stained karyotypes, the genus Hipposideros shows consider- Guinea or northeastern Queensland in Australia (Corbet able karyotypic conservatism, and for all but one species, 2n and Hill 1992; Koopman 1994). However, it is generally as- = 32 and the number of autosomal arms (EN) = 60. Rau- sumed that Australia was colonized by bats migrating from tenbach et al. (1993) suggested that the chromosomal com- Asia rather than &om South America (Hamilton-Smith plement of H. comrnersoni (2n = 52, FN = probably 60) may 1975; Flannery 1989; Hand et al. 1994). although their ap- have wolved from the most common hipposiderid state by pearance in Australia predates the hal breakup of Gon- 10 centric fissions, producing change in diploid number but dwana (Hand et al. 1994). The arrival of hipposiderids into not in fundamental number. On the basis of data on the New Guinea most probably occurred during the Miocene G-banded chromosomes, Sreepada et al. (1993) proposed (Hipposideros spp.) and Pliocene (AseUiscw hicuspldatus) that the ancestral lineage of Hipposideros derived from a (flannery 1990). rhinolophoid ancestor whose karyotype was siinilar to that To date it has been generally accepted that the family of R. Zuctus (2n = 32, EN = 60; Naidu and Gururaj 1984; originated somewhere in the Old World tropics, probably in Harada et al. 1985b; Hood et al. 1988). However, direct mcaor Asia (Koopman 1970; Sige 1991), and only recently comparison of the banding pattern in chromosomes of R. Hand et al. (1994) suggested, although indirectly, that it may luctus and Hipposideros spp. is not available. Homology of have evolved in the Southern Hemisphere. The Tertiary these karyotypes is thus not dear, and the arm combination karstic fissure-fills of western Europe show that from the in metacentric autosomes may differ. late Eocene to at least the middle Oligocene, hipposiderids Second, karyological data suggest that the autosomes for were the most diverse and numerous group of the cave- the ancestral karyotype in the sister-family Rhinolophidae dwelling bats and that their distribution in the past was contained all acrocentric elements with 2n = '62 and FN = Pkylogeny of the Hipposideridae 37

Table 2.3 Synopsis of Kayotypes of Hipposiderids

Speaes 2n PN X Y Reference

Ascnia hidenc Baker et al. 1974 Ascllivus swliakanus Harada et al. 1985a Clocoticpmivnli Rautenbach et al. 1993 Coelopsfithi And6 et a. 1980 : Hipposidcros anniger Hood et al. 1988; Qumsiyeh et al. 1988 Hipposidros arm Ray-Chaudhuri et al. 1971; Sreepada et al. 1993 Hipposidcros bicolor Ray-Chaudhwi and Pathak 1966 Hipposidnos cafn Peterson and Nagorsen 1975 Rautenbach et al. 1993 DuliC and Mutere 1974 Hipposidnos cmtinw Harada and Kobayashi 1980 Hipposidnos ciwacm Sreepada et al. 1993 Hipposidcros commmoni Rautenbach et al. 1993 Hipposidnos dindnna Harada and Kobayashi 1980 Hipposidcrosfilw Ray-Chaudhuriet al. 1971; Harada et al. 1985a; Hood et al. 1988 Sreepada er al. 1993 Handa and Kaur 1980 Hippodews hypophyllw Sreepada et al. 1993 Hipposidnos lankdiva Sreepada et al. 1993 Handa and Kaur 1980 Hipposidnos larvahcc Harada et al. 1982; Hood et al. 1988 Hipposideros Lkapli Harada et al. 1982; Hood et al. 1988 Hipposidnos pratti Zhang 1985 Hipposidnos spcorir Sreepada et al. 1993 DuliC 1984 (Figure 3) Handa and Kaur 1980 HipposidcTos terasmsic . And6 et al. 1980 Hipposidcros turpis And6 et al. 1980 Triamops pnsiclLc DuliC and Mutere 1977

Notu: Zn, diploid number of chromosomes; FN,rod number of autosomid arm; X. Y, suchromosomes (scares: A, aaoc~nic;M, metacentris SM, submetacenuic; ST, rub- telocennic). The karyotypes of HippoMnos ccrvinus, H. hypophynw and H. mat- were originally desaibed as chose of H.'&~w Muanmi.!, H. pomona, and H. ~znnigcr tcrasouir, rapectinly (reviewed by Jenkins and W 1981; Yoshiydd 1991; Kock and Bhat 1994).

60 (summarized by Zima et al. 1992; see also Bogdanowicz occurred during the evolution fiom the ancestral karyo- and Owen 1992). This interpretation also is supported by type to the karyotypes we hdtoday (Qumsiyeh et al. phylogenetic analyses of morphological characters (Bog- 1988). This assessment does not contradict phylogenetic danowicz and Owen 1992). An acrocentric composition of relationships suggested by the common-part-removed the primitive karyotype, and the trend toward low diploid cladogram and seems to be in partial agreement with the chromosome numbers, have also been suggested for the positions of mainly non-Hipposideros species shown in the families Phyllostomidae and Vespertilionidae (Baker and discrete-state dadogram. Theii karyotypes have probably Bickharn 1980). Third, a newly described fossil genus.Vay1at- undergone extensive Robertsonian and non-Robertsonian sia, although a member of the Hipposideridae, probably changes, which resulted in the variable number of chromo- represents the stem group of Rhinolophus (Sigk 1990). somes (2n = 30-50) and autosomal arms (FN = 56-62) (see In light of these considerations, it seems that the auto- Table 2.3). somes of the common ancestor of Rhinolophidae and Hip- posideridae consisted of all acrocenaics rathei than meta- Conclusions centrics and that the trend was toward low, rather than high, diploid numbers. A comparison between the G- Several standard and novel analyses of a morphological .= banded chromosomes of R. acuminatw and H. amiger also data set, supplemented with karyotypic information, were "indicated that some non-Robertsonian processes must have used in search of a robust hypothesis for the phylogeny and the center of origin of the bat family Hipposideridae. The ate, ventral view: (0) behind or at the level of posterior cur- results suggest that phylogenetic a5nities among Recent vature of palate bone; (1) anterior to posterior curvanye species are not expressed accurately by current systematic of palate bone; arrangements based on Hill's (1963) supraspecific group- Posterior nasal spine (i.e., spicule at the center of posterior edge of hard palate): (0) absent or inconspicuous; (1) well- ings and that the genus Hippoderos might be a paraphyletic developed. taxon. Morphological wersion analysis failed to reveal Foramen wale: (0) small; (1) medium-about half the size . any significant differences in morphological diversification . of glenoid fossa; (2) almost as large as glenoid fossa. The -- among hipposiderid faunas fiom four zoogeographic re- linear character transformation is hypothesized to be gions, and no center of origin could be inferred fiom the 0>1>2. analyses of phenetic data. Prom phylogenetic evidence, Type of cochlea: (0) phanaerocochlear; (1) ayptocochlear. . however, it appears that the fdymost probably origi- This character and its states correspond to those distin- . ' nated somewhere in the Oriental region. Our analyses also guished by Nwacek (1991), although some of our findings - suggest that the common ancestor of the sister-families differ; we found both states present in more species, and a Rhinolophidae and Hipposideridae had all acrocentric state different &omthat reported by Nwacek (1991) for sw- rather than metacenmc autosomes, and that these families eral species. independently followed a pattern of Robertsonian fusions, Least basioccipital width: (0) less than or equal to the least width of the sphenoidal bridge; (1) greater than the least with the result that low diploid numbers are the derived width of the sphenoidal bridge. condition in both lineages. Foramen magnum: (0) elliptical; (1) wal. The phylogenetic relationships suggested by this study Shape of hamular prokess of the pterygoids, lateral view: (Figures 2.1 and 2.3) are supported by metric and nonmet- (0) strongly notched; (1) weakly or not at all indented. ric morphological data and should be considered tentative, Size of hamular process of the pterygoids: (0) loig:practi- as working hypotheses. Future study must adopt the total- cally reaching glenoid fossa; (1) short. evidence approach, combining morphological, genetic, Anterior edge of the ascending mandibular ramus: (0) pos- and biochemical character sets and determining the most- terior to or at the middle of last upper molar; (1) anterior parsimonious outcome of the pooled matrix. We still have to the middle of last upper molar. a long way to go in the field of hipposiderid phylogeny, but, Position of mental foramen, lateral view: (0) anterior to or like Theseus in the Minotaur's labyrinth, we have few land- in the middle of first premolar; (1) posterior to the middle marks to guide us. of first premolar. Bone connection between angular and condyloid pro- cesses, lateral view: (0) strongly notched; (1) shallow. Appendix 2.1. Posterior cusp on upper canines (usually one-quarier to The 30 Characte'rs in the Parsimony one-half the height of canine): (0) absent; (1) present. Analysis of the Hipposideridae Heel of second upper molar: (0) welldeveloped; (1) incon- spicuous. Hornlike crest in middle of dorsal part of premaxillae: Shape of third upper molar, buccal view: (0) pentagonal; (0) absent; (1) present. (1) triangular. Location of greatest neurocranial breadth, dorsal view: Anterior segment (parastyle-paracone-mesostyle triangle) (0) anterior cranium or middle of cranium; (1) posterior of third upper molar, occlusal view: (0) almost as large as cranium. that of the second upper molar; (1) much smaller than that Position of braincase, excluding sagittal crest: (0) evidently of the second upper molar. higher than rostrum; (1) almost as high as or lower than Lobes on the lower inner incisors: (0) three full lobes; rostrum. (1) two full lobes plus a third, rudimentary lobe; (2) only Distance between mastoids: (0) less than or equal to zygo- two lobes. The linear character transformation is hypothe- matic breadth; (1) greater than zygomatic breadth. sized to be 0 > 1 > 2. Zygoma, lateral view: (0) not expanded at all to moder- Diastema between first lower inasors: (0) absent; (1) present. ately expanded; (1) expanded into a wide plate. Diasterna between the last lower incison and lower ca- Anterior end of sagittal crest: (0) extends to interorbital nines: (0) absent; (1) present. constriction; (1) extends past interorbital constriction. Horizontal ribs on outer paru of ears: (0) present; (1) absent. Lambdoidal crest: (0) absent or weak; (1) extremely well- Third metacarpal: (0) shorter than fifth metacarpal; developed. (1) longer than fifth metacarpal. Perforations behind nasal swellings: (0) zero to five foram-. Fourth metacarpat: (0) shorter than fifth metacarpal; ina present; (1) more than five foramina present. (1) longer than fifth metacarpal. Location of central portion of posterior border of hard pal- Tail: (0) well-developed; (1) rudimenta'iy. Phylogeny of the Hipposideridae 39

Appendix 2.2. Distribution of States for the 30 Characters within Taxa of the E4tmily Hipposideridae

Characters and their states are as defined in Appendix 2.1. For all characters, state 0 is plesiomorphic, and states 1 and 2 are apomorphic. In the data matrix shmhere, the letter "B" indicates that both states 0and 1 are present (this was coded as 7" in Hennig86), and a question mark means that the state is unknown.

Character

Ancestor 000000"000000000000000000000000 Anthops ornatus 00000001010000010001~0100000011 Asellia patrizii 00~0010~~0000000000~0~~0000~10- Asellia tridens OOlOOlOllOOBOOOOOOOl11:10000110 Aselliscus stoliczkanus 000000000010010100~100000l0110 Aselliscus tricuspidatus OOOOOOOOOO~OOBOOOO~~OOOOOBO~~O Cloeotis percivali 100000010120100101111000001110 Coelopsfrithi 0100000~1~2001000~0100000l1001 Coelops robinsoni O1O~OOO1112OOBOOO1O1OOOOO11OO1~~ Hipposideros abae 000000001000100000010000000110 Hipposideros anniger 00000010100~000000~0~O0100000110 Hipposideros ater 0001000000011000000000000000l0 Hipposideros beatus O00000000000~0O?OOO~O~OOOOOl~O Hipposideros bicolor OOOOOOOOlOOOBOOOOOOOOOOOOOOOlO Hipposideros cafler 00010000000B1000000100000B0110 Hipposideros calcaratus 000001000000~000000~00000000~0 Hipposideroscamerunensis OOOOOOOOO~OOOOOOOOOOOOOOBOO~~O Hipposideros cervinus 0000000001001000000~0000000~l0 Hipposideros cineraceus 0001000010000000000000000000l0 Hipposideroscommersoni OO~OO~~O~OOBOOOOBOOOO~OOBOO~~O Hipposiderosco~ophyllus 00000000000'000?010000100000100 Hipposideros curtus OOO~OOO~~~OB~OO,OOO~~OOOOOOOO~O Hipposideros cyclops OOOOOOOOO1OOOOOOOOOoOOOO~OOllO Hipposideros diadema 001000100000000000000~0~000~~0 Hipposideros dinops 001001~0~00000~0~000000~-000~~0 Hipposideros dyocorum 00000000~000~00000000000000~~0 Hipposiderosfuliginosus OOOOOOOO~OOB~OOOOOO~O~OOOOO~~O Hipposideros fulvus 000000001000000000000000000010 Hipposideros galeritus OOOOOOO~~~OOOB?OOOOOOOOOOOOO~~'~~ Hipposideroshalophyllus OOO~OOOO~O~O~O?OOOOOOOOOOOO~~O Hipposiderosinexpectatus OO~OO~~O.$~OOOO~OOOOOO~O~OOO~~O Hipposiderosjonesi 000~0001~~~0~00000~~0000000~~0 Hipposideros lankadiva OO~OO1~OOOOOOOOOOOOOO~OOOOO~lO Hipposideros larvarus 00000000~~0,00000~0000~0~000~~0 Hipposideros lekaguli OOOOOOOOO~OOOOOOOOOOOOOOOOOllO Hipposideros lylei OOOOoO~o~OoOOoOoOOoOOOOOOOO~lO Hipposiderosmacrobullatus 0 00 10 0 0 0 0 0 10 11 00 0 00 0 0 0 0 0 00 0 010 Hipposiderosmaggietaylorae 0 0 0o 00 0 0 10 00 10 00 0 0 0 10 0 0 00 0 00 10 Hipposideros marisae 000~0000~~~0~0?0000000000000~0 Hipgosideros megalotis OOO1OOOO1O1OOOOOOOO1OOOOOBOOlO

' Hipposideros muscinus ?000000000000000000000000000l0 Character

123456789111111111122222222223 Taxon (continued) 012345678901234567890

Hipposideros obscurus Hipposideros papua Hipposideros pomona Hipposideros pratti Hipposideros pygrnaeus Hipposideros ridleyi . Hipposideros ruber Hipposideros sabanus Hipposideros semoni Hipposideros speoris Hipposideros stenotis Hipposideros temsensis Hipposide'ros turpis Hippasideros wollastoni Rhinonycteris aurantius Triaenopsfurculus Triaenops persicus

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