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Home , Cryptodira, Dermatemydidae, Dermochelyidae, Kinosternidae, Kinosterninae, Staurotypus

Copein, 1983(4), pp. 918-932

Taxonomy and Phylogeny of the Higher Categories of Cryptodiran Based on a Cladistic Analysis of Chromosomal Data

John W. Bickham and John L. Carr

Karyological data are available for 55% of all cryptodiran including members of all but one . Cladistic analysis of these data, as well as con sideration of other taxonomic studies, lead us to propose a formal classification and phylogeny not greatly different from that suggested by other workers. We recognize 11 families and three superfamilies. The platysternid and staurotypid turtles are recognized at the familial level. Patterns and models of karyotypic in turtles are reviewed and discussed.

OVER the past 10 years knowledge of turtle and the relationship between the shell and pel karyology has grown to such an extent vic girdle. In the cryptodires ("hidden-necked" that the Testudines is one of the better turtles), the neck is withdrawn into the body in known groups of lower vertebrates (Bickham, a vertical plane and the pelvis is not fused to 1983). Nondifferentially stained karyotypes are either the plastron or carapace, whereas in the known for 55% of cryptodiran turtle species pleurodires ("side-necked" turtles) the pelvic and banded karyotypes for approximately 25% girdle is fused to both the plastron and carapace (Bickham, 1981). From this body of knowledge, and the neck is folded back against the body in as well as a consideration of the morphological a horizontal plane. Cope's suborder Athecae variation in the order, we herein present a gen includes only the and is no eral review of the cryptodiran karyological lit longer recognized. Most authors include the erature and a discussion of the evolutionary re Dermochelyidae among the (Gaff- lationships of the higher categories of ney, 1975a; Mlynarski, 1976; Wermuth and cryptodiran turtles. Although this paper focus Mertens, 1977; Pritchard, 1979). es on the Cryptodira (the largest suborder of A few authors recognize the Trionychoidea turtles), the also has been well stud (sensu Siebenrock, 1909) and/or the Chelo- ied in terms of standard karyotypes (Ayres et nioidea (sensu Baur, 1893) at a suprafamilial al., 1969; Gorman, 1973; Bull and Legler, 1980) rank equivalent with the Cryptodira and Pleu and a few have been studied with banding tech rodira (Boulenger, 1889;Lindholm, 1929; Mer niques (Bull and Legler, 1980). tens et al., 1934). The suborder Cryptodira is usedhere in the sense of Williams (1950) and Historical review of taxonomic relationships.—The subsequent authors and includes all living non- primary subdivisions of the order comprising pleurodiran turtles. the turtles have undergone a great many name The families of the suborder Cryptodira are changes and rearrangements over the last 100 arranged in various superfamilies by several au years. Cope (1871) presented an arrangement thors. The , Chelonioidea and of the families into suborders which is still widely Trionychoidea are superfamilies common to accepted today. Until Cope, the subordinal and most of the recent classifications (Williams, 1950; suprafamilial classification of turtles was pri Romer, 1966;Gaffney, 1975a; Mlynarski, 1976). marily based on differences in the digits among However, the limits of these taxa are not uni the sea turtles, the aquatic turtles and/or the formly agreed upon. terrestrial . Hoffman (1890) and Kuhn The non-trionychoid freshwater and land (1967) present reviews of the early classifica cryptodiran turtles include the , tions. , , Platysterni- Cope recognized the currently widely ac dae, and Testudinidae and are usu cepted suborders Cryptodira and Pleurodira. ally placed in the Testudinoidea (Williams, 1950; Two major differences between these two sub Romer, 1966). Gaffney (1975a) includes the orders are in the plane of retraction of the neck Kinosternidae and Dermatemydidae in the

© 1983 by the American Society of Ichthyologists and Herpetologists BICKHAM AND CARR—TURTLE CHROMOSOME PHYLOGENY 919

Trionychoidea. Mlynarski (1976) includes only ilies is difficult. The fact that a scale is in the the Emydidae and Testudinidae in the Testu- same position in members of different families dinoidea. He recognizes the superfamily Che- does not necessarily imply homology (Hutchi lydroidea to include the Chelydridae, Derma- son and Bramble, 1981). temydidae, Kinosternidae and Platysternidae. The Chelonioidea includes the Methods and the Dermochelyidae (Baur, 1893; Gaffney, 1975a). Williams (1950), Romer (1966), and Details for the procedures for turtle cell cul Mlynarski (1976) recognize a separate super- ture, chromosome preparation, and banding family, the Dermochelyoidea, for the family analysis have been published (Bickham, 1975; Dermochelyidae, and include only the Cheloni Bickham and Baker, 1976a; Sites et al., 1979b). idae in the Chelonioidea. Chromosomes were arranged, according to the The Trionychoidea usually includes both the method of Bickham (1975), into three groups and Carettochelyidae (Mlynarski, (A:B:C:) where group A included metacentric- 1976), but Williams (1950) and Romer (1966) submetacentric macrochromosomes, group B recognize the Carettochelyidae separately in the subtelocentric-telocentric macrochromosomes, Carettochelyoidea. and group C microchromosomes. The A:B:C: Most of the currently utilized family or formula is given after the diploid number in subfamily level taxa have been commonly rec Fig. 3 and in the text. ognized since Boulenger (1889). However, there This paper represents a synthesis and re- is no complete agreement regarding the level analysis of (mostly) published data. In reanalyz at which certain taxa should be recognized. Par ing the data we employed cladistic methodology sons (1968) reviewed this confusing situation (Hennig, 1966) in which sister groups were es with regard to the Chelydridae, Staurotypidae, tablished by the determination of groups that Kinosternidae, Platysternidae, Emydidae and possessed shared derived characters (synapo- Testudinidae, as recognized here. Not men morphies). Because banded karyotypes were not tioned by him are the inclusion of Platysternon available for the most appropriate outgroup in the Chelydridae (Agassiz, 1857; Gaffney, taxon (Suborder Pleurodira: Family ) 1975b) and the recognition of the Staurotypi we employed an "internal" method of character dae (Baur, 1891, 1893; Chkhkvadze, 1970). polarity determination. Specifically, characters The above discussion of the history of cryp- that were shared among families considered to todiran serves to illustrate the com be distantly related, known from the re plexity of the relationships of the inclusive taxa. cord to be early derivatives of the cryptodiran The taxonomic confusion seems to result from: radiation, or thought to be morphologically 1) extensive convergent evolution in certain primitive, were considered as primitive (plesio- morphological traits, 2) the failure of some morphic) chromosomal characters. Because of workers to distinguish between shared primi the nature of karyotypic variation in cryptodires tive and shared derived character states and 3) the analysis was rather straightforward. For ex the lack of a widely accepted phylogeny of tur ample, dermatemydids are among the most tles. Chromosomal data are used in this paper primitive living turtles and their fossil history in an attempt to solve some of the evolutionary extends back to the , as does the che- and classificatory problems. Cytogenetic infor loniids which are thought to be an early offshoot mation seems useful at this level because of the of the cryptodiran line. These two families pos high degree of conservatism expressed in che- sess species with apparently identical karyo lonian karyotypes (Bickham, 1981). Addition types. It is highly unlikely that these two families ally, the application of chromosome banding possess a synapomorphy at this level of the phy techniques solves one of the most troublesome logeny. This would mean that these two families problems in phylogeny reconstruction; namely, were more closely related to each other than to the determinationof homologous characters. any other families studied, an arrangement that When two chromosomes have identical banding appeared to conflict with everyother line of patterns it can safely be concluded that they are evidence in the literature. We therefore con homologous. It is sometimes difficult to deter sidered this karyotype to be primitive, at least mine homology among morphological charac for the non-trionychoid families, and the karyo ters. For example, determination of homologies types of other families were derived from this among the plastral scales of various turtle fam (see below). 920 COPEIA, 1983, NO. 4

*l It*

MM #;*

B II 1! ft*

#■#

Fig. 1. G-band karyotype of a batagurine emydid (Chinemys reevesi, 2n = 52). The chromosomes are ar ranged into group A (metacentric or submetacentric macrochromosomes), group B (telocentric and subtel- ocentric macrochromosomes), and group C (microchromosomes).

is unclear (Bickham and Baker, 1976a). There Results and Discussion is no karyotypic evidence to indicate emydines The following discussion is segmented into are at all closely related to , the the commonly accepted family groups. In gen only New World batagurine (Carr, 1981). eral, we have accepted each of the families as There may be some hint of the batagurine-emy- distinct entities and do not question their valid- dine transition in the finding of severalspecies ity. of Asiatic batagurineswith 2n = 50 (Table 1). Any relationship of the emydines to the 2n = Emydidae.—The two subfamilies of emydid tur 50 batagurines will require evidence from other tles are characterized by different karyotypes. character systems in order to establish its exis

The predominantly New World emydines have tence. 2n = 50 and the predominantly Old World ba- tagurines mostly have 2n = 52 (Table 1). A few Testudinidae.—The karyology of this family is batagurine species also possess 2n = 50 (Table not as well studied as that of the Emydidae but 1), including crassicollis, the only it seems certain that the primitive karyotype is emydid known to possess sex chromosomes (Carr 2n = 52. Some species are known to possess G- and Bickham, 1981). Bickham and Baker (1976a) band patterns identical to those of certain ba concluded that the primitive karyotype of the tagurines including pardalis, G. elon- Emydidae was 2n = 52 and identical to that of gata and G. elephantopus (Dowler and Bickham, bealei and other Old World batagurines. 1982). C-band variation exists among species of This has been supported by recent findings that Geochelone, and the karyotypes ofGopherus some testudinids have banded karyotypes iden species differ from Geochelone species by the tical to those of Chinemys reevesi and other ba morphology and location of the nucleolar or tagurines (Dowler and Bickham, 1982). Fig. 1 ganizing region (NOR) (Dowler and Bickham, illustrates the karyotype of a batagurine (Chi 1982). Although this family is nearly world-wide nemys reevesi) that possesses the proposed prim in distribution and morhpologically diverse, the itive emydid karyotype. available data indicate a high degree of karyo- The origin of the 2n = 50 emydine karyotype logical conservatism. BICKHAM AND CARR—TURTLE CHROMOSOME PHYLOGENY 921

Table 1. Diploid Numbers of Cryptodiran Turtles. Each reference is listed under the currently rec ognized name if different from that under which it was originally reported. Unpublished data have been processed in our lab.

Diploid Taxon number Source

Matthey, 1930, 1931; Wickbom, 1945; Polli, 1952; Matthey and Van Brink, 1957; Van Brink, 1959; Ivanov, 1973

Van Brink, 1959; Forbes, 1966; Killebrew, 1977a Glascock, 1915; Van Brink, 1959; Forbes, 1966; Stock, 1972; DeSmet, 1978

Forbes, 1966

Jordan, 1914; Forbes, 1966 Forbes, 1966; Stock, 1972; Bickham and Baker, 1976a; Killebrew, 1977a DeSmet, 1978 Stock, 1972 Killebrew, 1977a DeSmet, 1978 Forbes, 1966; Gorman, 1973; Bickham and Bak er, 1979 Forbes, 1966 Killebrew, 1977a Stock, 1972; unpublished Killebrew, 1977a Gorman, 1973 Gorman, 1973; Killebrew, 1977a Gorman, 1973; Bickham and Baker, 1976a, b, 1979 Bickham and Baker, 1976a, b Unpublished Bickham and Baker, 1976a, b Forbes, 1966; McKown, 1972; Killebrew, 1977a Forbes, 1966; Stock, 1972; Bickham and Baker, 1979

Forbes, 1966; McKown, 1972 McKown, 1972; Killebrew, 1977a McKown, 1972; Stock, 1972; Killebrew, 1977a McKown, 1972 Killebrew, 1977a

McKown, 1972 McKown, 1972; Unpublished McKown, 1972; Killebrew, 1977a McKown, 1972; Killebrew, 1977a McKown, 1972; Killebrew, 1977a McKown, 1972; Killebrew, 1977a Stock, 1972; Bickham and Baker, 1976a; Kille brew, 1977a 922 COPEIA, 1983, NO. 4

Table 1. Continued.

Diploid Taxon number Source

T. Carolina [32]* Jordan, 1914 50 Forbes, 1966; Huang and Clark, 1967; Clark et al., 1970; Stock and Mengden, 1975; Bickham and Baker, 1979

T. c. triunguis 50 Forbes, 1966; Stock, 1972; Killebrew, 1977a

T. coahuila 50 Killebrew, 1977a Deirochelys reticularia 50 Stock, 1972; Killebrew, 1977a

D. r. chrysea 50 Forbes, 1966

Malaclemys terrapin 50 Forbes, 1966; Stock, 1972

M. L littoralis 50 McKown, 1972 Emydoidea blandingi 50 Forbes, 1966; Stock, 1972

Clemmys insculpta 48 Forbes, 1966 50 Stock, 1972; Bickham, 1975, 1976

C. guttata 48 Forbes, 1966 50 Stock, 1972; Bickham, 1975

C. m. marmorata 50 Stock, 1972; Bickham, 1975 C. m. pallida 50 Killebrew, 1977a

C. muhlenbergi 50 Bickham, 1975

BATAGURINAE Sacalia bealei 52 Bickham, 1975; Bickham and Baker, 1976a caspica leprosa 50 Killebrew, 1977a 52 Bickham, 1975, 1976

M. c. rivulata 52 Bickham, 1975, 1976

M. mutica 52 Nakamura, 1935, 1937,1949; Stock, 1972; Gor man, 1973; Bickham, 1975; Killebrew, 1977a

M. japonica 52 Nakamura, 1935; Sasaki and Itoh, 1967; Becak et al., 1975 Bickham and Baker,1976a, b Barros et al., 1975; Bickham and Baker, 1976a, b Killebrew, 1977a Killebrew, 1977a; Carr, 1981

Carr, 1981

Carr, 1981 Nakamura, 1937, 1949 DeSmet, 1978; Carr, 1981 DeSmet, 1978 Sasaki and Itoh, 1967, Takagi and Sasaki, 1974; Killebrew, 1977a; Sites et al., 1979a; Dowler and Bickham, 1982; Haiduk and Bickham, 1982 Gorman, 1973 Nakamura, 1949; Stock, 1972; Killebrew, 1977a; DeSmet, 1978; Haidukand Bickham,1982

Carr, 1981 Gorman, 1973 BICKHAM AND CARR—TURTLE CHROMOSOME PHYLOGENY 923

Table 1. Continued.

Diploid Taxon number Source

C. flavomarginata

Kachuga tecta

K. smithi

K. trivittata

K. dhongoka

Ocadia sinensis

Malayemys subtrijuga

Orlitia borneensis

Siebenrockiella crassicollis

Callagur borneoensis

Hieremys annandalei

TESTUDINIDAE

Gopherus agassizi 52 Atkin et al., 1965; Ohno, 1967, 1971; Huang and Clark, 1969; Jackson and Barr, 1969; Stock, 1972; Gorman, 1973

G. berlandieri 52 Stock, 1972; Gorman, 1973; Killebrew and McKown, 1978; Dowler and Bickham, 1982

G. polyphemus 54 Forbes, 1966

52 Dowler and Bickham, 1982

Kinixys belliana belliana 52 Killebrew and McKown, 1978

Testudo hermanni 52 Stock, 1972

T. graeca 52 Huang and Clark, 1969; Clark etal., 1970; Shin- darov et al., 1976

54-60 Matthey, 1930 Geochelone denticulata 52 Sampaio et al., 1969,1971; Bickham, 1976; Bickham and Baker, 1976a, b Forbes, 1966; Sampaio etal., 1971; Stock, 1972; Bickham and Baker, 1976b Unpublished Goldstein and Lin, 1972; Benirschke et al., 1976; Dowler and Bickham,1982 DeSmet, 1978; Dowlerand Bickham,1982

Dowler and Bickham, 1982 Benirschke et al., 1976

Dowler and Bickham, 1982

Gorman, 1973; Haiduk and Bickham, 1982

Bull et al., 1974; Moon, 1974 Gorman, 1973 Bull et al., 1974; Moon, 1974; Killebrew, 1975 924 COPEIA, 1983, NO. 4

Table 1. Continued.

Diploid Taxon number Source

56 Gorman, 1973

S. salvini 54 Bull et al., 1974; Moon, 1974; Sites et al., 1979a, b

CHELYDRIDAE

Chelydra s. serpentina 52 Forbes, 1966; Stock, 1972; Gorman, 1973; Bick ham and Baker, 1976a; Killebrew, 1977b; DeSmet, 1978

C. s. os ceo I a

C. s. acutirostris

Mac rod em ys tern m inckii

KINOSTERNIDAE

Kinosternon flavescens

K. sub rub rum

K. s. hippocrepis

K. s. steindachneri

K. leucostomum

K. I. postinguinale

K. hirtipes

K. integrum

K. herrerai

K. scorpioides

K. s. scorpioides

K. s. carajasensis

K. s. abaxillare

K. s. cruentatum

K. bauri

Sternotherus odoratus

S. carinatus

S. minor

DERMATEMYDIDAE

Dermatemys mawii

CHELONIIDAE

Caretta caretta

Chelonia my das

Eretmochelys imbricata BICKHAM AND CARR—TURTLE CHROMOSOME PHYLOGENY 925

Table 1. Continued.

* Reported as N = 16.

Platysternidae.—The standard karyotype of the element in emydids and testudinids (and pla- single species of platysternid (Platysternon meg tysternids based on standard chromosome mor acephalum) has 2n = 54 (Haiduk and Bickham, phology). This chromosome is acrocentric in 1982). This species appears to have close affin chelydrids, kinosternids, dermatemydids and ities to the Emydidae but is karyotypically dis cheloniids (Fig. 2). We conclude that the biarmed tinct from all emydids thus far studied. Because condition is derived. Centric fusion of the an P. megacephalum and emydids do apparently have cestral acrocentric macrochromosome with a synapomorphic chromosomes that are not microchromosome accounts for the presence of shared with chelydrids, Haiduk and Bickham a subtelocentric macrochromosome in the com (1982) considered P. megacephalum to comprise mon ancester of the Emydidae, Testudinidae, a family distinct from the Chelydridae (sensu Platysternidae and Staurotypidae. This is indic Gaffney, 1975b) and resurrected the Platyster ative of the staurotypids belonging to a clade nidae (Gray, 1870), a move also suggested by that does not include kinosternids ( Whetstone (1978). and ). This seems irreconcilable with

Staurotypidae.—This group is usually consid ered to be a subfamily (Staurotypinae) of the Kinosternidae. Standard karyotypes of all three species in this group are known (Table 1; see especially Bull et al., 1974). The two species of are distinctive in possessing an XX/ XY sex chromosome system (Bull et al., 1974; Sites et al., 1979a). Claudius angustatus, like nearly all other turtle species studied, does not possess heteromorphic sex chromosomes but Fig. 2. G-band patterns of the second group B chromosomes of (left to right) a staurotypid, an emy- appears to be otherwise karyotypically identical did, a kinosternid and a cheloniid. The long arms of to Staurotypus (Bull et al., 1974). Sites et al. all 4 taxa are identical; the short arms of the stau (1979a, b) report banded karyotypes of 5. sal- rotypid and emydid are euchromatic and identical, vini and show that this species possesses a however, the short arms of the kinosternid and the biarmed second group B macrochromosome cheloniid are small and heterochromatic; see text for that appears to be homologous to an identical further discussion. 926 COPEIA, 1983, NO. 4 the current classification; it is therefore pro stantiated by recent studies using current tech posed that the Staurotypinae be elevated to fa niques. milial rank. Trionychidae.—Members of both subfamilies Chelydridae.—Thetwo extant species of this ( and ) have 2n = family have been studied for both standard (Ta 66 (Table 1). Reports of other diploid numbers ble 1) and banded karyotypes (Haiduk and Bick- have been unsubstantiated in subsequent stud ham, 1982). serpentina and Macroclemys ies. The report of 2n = 52-54 in leithii temminckii bothhave 2n = 52 but differ in the (Singh et al., 1970) was due to the misidentifi- morphology of certain chromosomes. Haiduk cation of this specimen (Kachuga dhongoka, Em- and Bickham (1982) conclude that these two ydidae; Singh, 1972). The 2n = 66 karotype was species do not share any derived chromosomal considered by Bickham et al. (1983) to be the characteristics with each other orwith any oth primitive karyotype for the family. Banding er families of Cryptodira. However, thekaryo- comparisons between Trionyx and Chelonia re type of M. temminckii could be derived from that vealed little homology between the Trionychi of C. serpentina. The latter is considered the dae and Cheloniidae (Bickham et al., 1983). primitive karyotype for the family. Carettochelyidae.—The single extant species Kinosternidae.—This family is comprised of two (Carettochelys insculpta) has 2n = 68 (Bickham et genera and about 18 species and has been well al., 1983). Although no banding data have been studied karyotypically (Table 1). Early, and ap reported for this species, the standard karyo parently inaccurate, reports aside (Table 1), all type is very similar to the 2n = 66 karyotype of species thus far examined appear to possess trionychids. 2n = 56. Banded karyotypes (Bickham and Bak er, 1979; Sites et al., 1979b) indicate all species Taxonomy.—The acceptability of using karyo- possess a large, subtelocentric macrochromo- typic data in order to draw phylogenetic infer some not found in any other group of turtles. ences and erect a classification at the level of Kinosternids do not share any derived chro family and higher is based upon the conserva mosomal characters with any other turtle fam tism of the karyotypic character system. By ily, including the staurotypids with which they character system, we refer to a suite of char are usually considered confamilial. An interest acters and character states which may be pre ing variation was found in this family by Sites sumed to be closely enough related to be within etal. (1979b). Heterochromatin that stains dark the realm of influence of the same set of evo in both G- and C-band preparations was found lutionary constraints. According to this line of in Sternotherus minor, Kinosternon baurii and K. resasoning then, karyotypic data constitute a subrubrum, but not found in K. scorpioides. The character system separate from the character presence of this type of heterochromatin was systems associated with electrophoretic data or considered to be a derived character (it is not cranial osteology, etc. The level at which char found in closely related families) shared among acters are relatively constant within a group is the three species that possess it, indicating that the point at which those characters are of sys the genus Sternotherus has affinities with tem tematic utility and those characters are said to perate species of Kinosternon. be conservative (Farris, 1966). Our studies and a reviewof the pertinent literature indicate that Dermatemydidae.—The single extant species of family level groups within the Cryptodira are this family (Dermatemys mawii) possesses 2n = 56 characteristically karyotypically homogeneous (Table 1). There are no uniquely derived ele and that the significant variation (in the phy ments and this species shares no derived chro logenetic sense) is observable interfamilially. It mosomes with any other family. is upon these premises that we propose the clas sification in Table 2 based upon our cladistic Cheloniidae.—Members of this family possess analysis of the karyotypic data. 2n = 56 (Table 1). Banding data indicate che- This classification is conservative in that all loniids and dermatemydids are karyotypically families commonly recognized are maintained, indistinguishable (Bickham et al., 1980; Carr et even though in two instances there are family al., 1981). Early reports of other diploid num pairs which we cannot karyotypically distin bers and sex chromosomes have not been sub guish [i.e., Cheloniidae-Dermatemydidae and BICKHAM AND CARR—TURTLE CHROMOSOME PHYLOGENY 927

Table 2. Taxonomic Arrangement of the High er Categories of Cryptodiran Turtles.

Suborder Cryptodira Superfamily Chelonioidea Family Cheloniidae Family Dermochelyidae Superfamily Testudinoidea Family Emydidae Family Testudinidae Family Platysternidae Family Staurotypidae Family Chelydridae Family Kinosternidae Family Dermatemydidae Fig. 3. Cladogram showing the hypothesized re Superfamily Trionychoidea lationships of the higher categories of cryptodiran Family Trionychidae turtles. The diploid number and the number of chro mosome pairs in groups A:B:C (Fig. 1) in the proposed Family Carettochelyidae primitive karyotype of each family (and both subfam ilies of Emydidae) are shown. Because the trionychoid families are so divergent, the A:B:C formulas are not given (Bickham et al., 1983). Characters 1 -5 are listed Testudinidae-Emydidae (in part)]. The classifi and discussed in the text. cation departs from those that are commonly accepted in several respects, two of which de serve further attention. The first is the removal of the Dermatemydidae and Kinosternidae (plus to recognize the Staurotypinae as a separate Staurotypidae as herein conceived) from the family, the Staurotypidae. This conclusion is in- Trionychoidea (sensu GafFney, 1975a). Al congruent with data from other character sys though Gaffney (197 5a) and Zug( 1971) present tems. Many morphological studies report sim morphological evidence for a relationship be ilarities between the Kinosternidae and tween these groups, the karyotypic evidence Staurotypidae (among these Williams, 1950; clearly indicates that these groups are from lin Parsons, 1968; Zug, 1971). Most such studies eages which have been separated for a long pe have not attempted cladistic analyses (two ex riod of time. No karyotypic apomorphies are ceptions are Gaffney, 1975; Hutchison and shared between the Trionychoidea, and the Bramble, 1981). There seems no obvious or Dermatemydidae and Kinosternidae and in fact simple manner in which to reconcile the con few symplesiomorphies remain (Bickham et al., flicting data from the karyotypic character sys 1983;Carretal., 1981). tem and the overwhelming amount of data from The Staurotypidae as herein recognized de various morphological character systems. In serves special attention. The karyotypic data recognizing the Staurotypidae, we have made clearly indicate not only a relatively large karyo explicit our prediction of its relationships to typic distance between the commonly recog other testudinoid families. Independent confir nized and Staurotypinae, but also mation or refutation of these relationships will a clearly identifiable difference in direction of determine the merit of this move. karyotypicevolution in that the Staurotypidae The three superfamilies are all considered to can be allied synapomorphically in a derived be holophyletic. Fig. 3 presents a cladogram clade which does not include the Kinosternidae. that we believe best reflects the branching se Even if a karyotypic convergence on the apo- quence of theevolution of this group. The Tes morphic character allying the Staurotypidae tudinoidea and Chelonioidea may be sister with the Platysternidae, Testudinidae, and groups but this is as yet unproved. The primi Emydidae has occurred, the fact remains that tive karyotypes of these two taxa are identical, the Kinosternidae and Staurotypidae would still 2n = 56 (character 1 in Fig. 3), and very differ be karyotypically distinct (and nonrelatable), at ent from that of the Trionychoidea, 2n = 66- least to as great a degree as are any of the other 68 (character 2 in Fig. 3), but we do not yet families. In the context of this paper and our know the polarity of these character states data-base we are left with no recourse except (Bickham et al., 1983). 928 COPEIA, 1983, NO. 4

All testudinoid and chelonioid turtles possess didae in the Trionychoidea (Gaffney, 1975a). at least seven group A macrochromosomes The chromosomal data do not support such an (character 1 in Fig. 3). Among the testudinoid arrangement because of the disparity in diploid families, a clade that includes Staurotypidae, number and chromosome morphology between Platysternidae, Testudinidae, and Emydidae can testudinoids (including kinosternids and der be identified by the presence of a biarmed sec matemydids) and trionychoids (Bickham et al., ond group B macrochromosome (character 3 1983). in Fig. 3; Fig. 2). Another clade includes the Platysternidae, Testudinidae and Emydidae all Chromosomal evolution.—We conclude, for two of which primitively possess nine group A mac reasons, that the primitive karyotype of the sub rochromosomes (Fig. 1; character 4 in Fig. 3). order Cryptodira is most likely the 2n = 56 A clade including the Emydidae and Testudin karyotype of cheloniid and dermatemydid tur idae is characterized by a 2n = 52 9:5:12 prim tles. First, these are among the most ancient itive karyotype (Fig. 1; character 5 in Fig. 3). families in the suborder (both date from the Species of the emydid subfamily all Cretaceous), and second, this karyotype is high possess a karyotype derived from the primitive ly generalized and could have given rise to the 9:5:12 arrangement (Bickham and Baker, diversity ofkaryotypes in the suborder by a min 1976a). imum number of events. A primitive karyotype The Dermatemydidae, Kinosternidae and more similar to that of trionychoid turtles (2n = Chelyridae possess no chromosomal synapo- 66-68) cannot entirely be ruled out (Bickham morphies and the branching sequence of these et al., 1983). Comparisons with karyotypes of families is not obvious from chromosomal, mor the species of Pleurodira do not solve the prob phological or serological data. However, the lem because species of the Chelidae are known Chelydridae is usually considered to be most to possess diploid numbers in the 2n = 56 range closely related to the Emydidae (McDowell, as well as the 2n = 66 range (Bull and Legler, 1964; Zug, 1971;Frair, 1972; Haiduk and Bick 1980). However, the primitive karyotype of the ham, 1982) and the dermatemydids, morpho Pleurodira was considered by Bull and Legler logically one of the most primitive families of (1980) to be 2n = 50-54 which is consistent with turtles, are considered closely allied to the Kin our hypothesis of a 2n = 56 ancestral karyotype osternidae (Zug, 1971; Frair, 1972; Gaffney, for the Cryptodira. 1975b). If the above hypothesis is true, then chro The Cheloniidae and Dermochelyidae are mosomal evolution in the Trionychoidea in considered to comprise the suborder Chelo- volved an increase in the diploid number by a nioidea. There are no karyotypic data available reduction in the number of macrochromosomes for Dermochelys coriacea so the relationship be and an increase in the number of microchro- tween this species and cheloniids has yet to be mosomes. However, chromosomal evolution in tested chromosomally. But, these two families the Testudinoidea reduced the diploid number are closely related morphologically and sero- by an increase in the number of macrochro logically (Frair, 1979). We follow most other mosomes and reduction of the number of mi- workers in giving this group full superfamilial crochromosomes. status, recognizing that they have invaded an Bickham and Baker (1979) note that species adaptive zone, the marine environment, that is within a family or subfamily possess identical or distinctly different from that of most other tur very similar karyotypes. However, karyotypic tles. It must be emphasized that Chelonia mydas comparisons among families and subfamilies al (Chelonioidea) and Dermatemys mawii (Testudi- most always reveal variation. A more refined noidea) appear karyotypically identical and we analysis of the pattern of karyotypic variation interpret this to be the primitive karyotype of in turtles (Bickham, 1981) suggests that the rate these two superfamilies. of karyotypic evolution has decelerated and that The superfamily Trionychoidea includes only Mesozoic turtles evolved at a rate twice as fast the Trionychidae and Carettochelyidae. These as their descendants. Additionally, the kinds of two taxa are closely related chromosomally as chromosomal rearrangements incorporated well as morphologically and their karyotypes during the diversification of cryptodiran fami are distinctly different from those of species of lies differ from the kinds of rearrangements in the other two superfamilies. Some workers have corporated during the evolution of modern included the Kinosternidae and Dermatemy species. BICKHAM AND CARR—TURTLE CHROMOSOME PHYLOGENY 929

The above described pattern of karyotypic often are found in isolated stock tanks, , evolution is consistent with the canalization intermittent streams andpermanent springs. model of chromosomal evolution (Bickham and Population sizes are often small and there is Baker, 1979). Under this model, evolution of probably very little migration among popula the karyotype is driven by natural selection be tions. cause the chromosomal rearrangements alter Many of the above mentioned biological char genetic regulatory systems. Changes that are acteristics of turtles conceivably could promote adaptive accumulate more rapidly during the chromosomal speciation. That it does not occur early radiation of a lineage. As time goes on in a major radiation (Cryptodira) does not mean more and more adaptive linkage groups are that the process is not viable in other taxa, but produced. Further chromosomal rearrange its absence is somewhat unexpected. In conclu ment tends to break up adaptive gene sequences sion, population parameters are poorly corre and the rate of chromosomal evolution slows lated with chromosomal variability in turtles and down. Thus, in an ancient group such as turtles, in principle we agree with the criticisms of the the process of canalization has had such a long chromosomal speciation models espoused by period of time to act that karyotypic evolution Bickham and Baker (1979, 1980) and Futuyma among modern forms is virtually nonexistent. and Mayer (1980). However, when karyotypic comparisons are made of taxa that diverged early during turtle Acknowledgments evolution, such as comparisons of the primitive karyotypes of families, variation is found to be Our work on turtle karyology has been fund more pronounced. ed by the National Science Foundation under Models that explain karyotypic evolution by grants DEB-7713467 and DEB-7921519. We population demography, such as deme size, do are grateful to the numerous people who have not apply to turtles. The classical model of chro provided us with technical assistance, or spec mosomal speciation (White, 1978) requires fix imens used in our analyses, including: T. W. ation of chromosomal rearrangements in small Houseal, K. Bjorndal, E. O. Moll, F. L. Rose, demes due to genetic drift or inbreeding. There J. M. Legler,J.J. Bull, R. C. Dowler andM. W. is some question as to whether chromosomal Haiduk. Instructive comments on the manu speciation is in fact a viable process (Bickham script were received from D. M. Bramble, J. H. and Baker, 1979, 1980; Futuyma and Mayer, Hutchison and J. M. Legler. 1980), but even if it is, it certainly is not oper ative in turtles. There are no known chromo Literature Cited somal races in turtles. This could be explained by turtles characteristically not having small Agassiz, L. 1857. Contributions to the natural his population sizes or other demographic factors tory of the United States of America. First mono that promote the fixation of chromosomal rear graph in three parts. II. North American Testu- rangements by genetic drift or inbreeding. dinata: 235-452d. However, turtles display such a diversity of de Atkin, N. B., G. Mattinson, W. Becak and S. Ohno. 1965. The comparative DN A content of 19 species mographic characteristics (Auffenberg and of placental mammals, , and birds. Chro- Iverson, 1979; Bury,1979; Bustard, 1979) that mosoma 17:1-10. this explanation seems untenable. Auffenberg, W., and J. B. Iverson. 1979. Demog Turtles exhibit a diverse array of morpho raphy of terrestrial turtles, p. 541-569. In: Turtles: logical types and occur in nearly all habitats Perspectives and research. M. Harless and H. Mor- available to reptiles. Some, such as the migra lock (eds.). John Wiley and Sons, New York. tory sea turtles, arehighly vagile but others, Ayres, M., M.M. Sampaio, R. M. S. Barros, L. B. such as tortoises, have relatively low vagility. Dias andO. R. Cunha. 1969. A karyological study Reproductive rates also vary. The turtle of turtles from the Brazilian Amazon region. Cy- may lay as many as 200 in a single clutch, togenetics 8:401-409. Barros, R. M., M. Ayres, M. M. Sampaio, O. Cunha some emydids may lay only a single large . and F. Assis. 1972. Karyotypes of two While there are certainly many species that of turtles from the Amazon region of Brazil. Car- characteristically have large population sizes, we yologia 25:463-469. can point to many that probably do not. For , M. M. Sampaio, M. F. Assis, M. Ayres and example, kinosternids and emydids that occur O. Cunha. 1975. A karyological study of in the arid western United States and punctularia punctularia (Daudin, 1802) from the 930 COPEIA, 1983, NO. 4

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