Biology_of_Turtles

within parareptiles, but it is important to recognize that all of the aforementioned cladistic analyses were based on the presupposition that turtles are stem reptiles. The consequence was that if any diapsid was included in the analysis, it was the Paleozoic stem-diapsid Petrolacosaurus (Reisz, 1981). This implicitly placed greater weight on “anapsid” characters at the cost of characters that turtles might share with crown-group diapsids (Sauria).

However, there had been a number of earlier authors who had questioned the anapsid status of turtles and who considered them to be diapsids instead. Goodrich (1916, 1930) was one of the first to point out that reptiles would not form a natural group unless they were grouped with birds within Sauropsida. He thought turtles ought to be included in this group as well, and on this basis concluded that the temporal region in the turtle skull must have been secondarily closed. Boulenger (1918) added to the debate his observations that revealed differences of detail in the structure of the temporal region of the skull in the captorhinomorphs and in the oldest known fossil turtle, Proganochelys, from the early Late Triassic of Germany. Broom (1924) emphasized the striking similarities in the pelvic girdle and hind limbs that are shared by turtles and diapsid lepidosaurs such as Sphenodon (Rieppel, 1995). Lakjer (1926) believed the lower temporal arch to have been reduced to the quadrato-maxillary ligament in the modified diapsid skull of squamates and considered turtles to be modified diapsids as well, based on the presence of a quadrato-maxillary ligament in that group. In contrast, Rieppel (1990) found no support for diapsid affinities of turtles in the structure of the trigeminal jaw adductor musculature. DeBeer (1937) used developmental data concerning the occipito-atlantal joint to justify his hypothesis that turtles are related to (diapsid) archosaurian reptiles. Hofsten (1941) seconded that view and postulated a relationship of turtles with crocodiles and birds on the basis of the presence of a secondary subclavian artery. The hypothesis of archosaurian affinities of turtles earned significant subsequent support, again mostly on the basis of cladistic argumentation (Ax, 1984; Gardiner, 1993; Hennig, 1983; Lovtrup, 1977, 1985; Remane, 1959; see the discussion in Rieppel, 2000a). It is interesting to note that a diapsid status of turtles was accepted almost exclusively by zoologists, whereas their status as anapsid reptiles remained the consensus view among paleontologists (Romer, 1956, 1968; Kuhn-Schnyder, 1980).

13.3The Recent Revival of the Debate

The issue of turtle relationships within amniotes was brought back to center stage by Lee’s studies (1993, 1995, 1996, 1997a), who found turtles to be nested within the pareiasaurs and, on that basis, developed an evolutionary scenario for the gradual derivation of the turtle body plan from that of a derived pareiasaur such as Anthodon. Key elements of that evolutionary scenario are the derivation of the turtle shell from osteoderms and a posterior shift of the pectoral girdle that would result in a morphological position of the scapula inside the rib cage. Whereas plausible from a gradualisticphylogenetic perspective, this scenario does not explain the morphological complexity of the turtle carapace (Goette, 1899; Burke, 1989; Rieppel & Reisz, 1999; Rieppel, 2001; Gilbert et al., 2001; Gilbert et al., 2004; Kuraku et al., 2005), nor is it supported by turtle ontogeny, which shows no indication of a backward shift of the pectoral girdle (Ruckes, 1929; Burke, 1991; Rieppel, 1996). The conclusion had to be that “developmental specialization does not provide any hint as to the way in which this pattern evolved phylogenetically” (Carroll, 1988).

Lee’s (1995, 1997a) phylogenetic hypothesis of preiasaurian relationships of turtles (Figure 13.1) and the evolutionary scenario based on it (Lee, 1993, 1996) were challenged by the finding that turtles could be the sister-group of a clade of Triassic marine reptiles, the Sauropterygia (Rieppel, 2000b), both groups nesting at the base of the lepidosauromorph lineage of the diapsid tree (Rieppel, 1994; Rieppel & DeBraga, 1996; DeBraga & Rieppel, 1997; Rieppel & Reisz, 1999). These results conflict with those of Merck (1997; see also the discussion in Brochu, 2001), whose analysis showed turtles again to group with Triassic marine reptiles (in this case ichthyosaurs, sauropterygians, and thalattosaurs) but all of them nesting at the base of the archosauromorph clade of the diapsid radiation (Figure 13.1).

The increased interest in turtle relationships as reflected by these morphological studies triggered a series of molecular studies that all confirmed the archosaurian affinities of turtles (Platz & Conlon, 1997; Gorr et al., 1998; Kirsch & Mayer, 1998; Zardoya & Meyer, 1998; Hedges & Poling, 1999; Kumazawa & Nishida, 1999; Mannen & Li, 1999; Mindell et al., 1999; Cao et al., 2000; Page, 2000; Janke et al., 2001; Li & Tsoi, 2002; Rest et al., 2003; Iwabe et al., 2005). However, there was variation in the relative relationships of turtles, crocodiles, and birds as indicated by DNA data: some studies found crocodiles to be the sister taxon of turtles (supported primarily by nuclear data), whereas in other analyses turtles were found to be the sister-group of a clade comprising crocodiles and birds, supported primarily by mitochondrial genes (Iwabe et al., 2005).

Problems of the molecular analyses of turtle relationships, possibly responsible for the partial incongruence of the signals obtained, were identified as long-branch attraction, taxon sampling, and rate heterogeneity among the genes employed (Brochu, 2001). Incongruent signals for turtle relationships based on morphological data were attributed to different philosophies “regarding how different types of data should be handled in phylogeny reconstruction” (Hill, 2005; for further discussion of that issue, see Rieppel & Kearney, 2006; Harris et al., 2007). Lee (2001) presented a simultaneous analysis (Nixon & Carpenter, 1996) that combined osteological data with characters of the soft anatomy taken from Gauthier et al. (1988) and with the mitochondrial DNA data from Zardoya and Meyer (1998; data modified as described by Lee, 2001). Whereas the analysis of the molecular data alone showed turtles to group with archosaurs (Lee, 2001, fig. 5; congruent with Zardoya & Meyer, 1998), as did the combined analysis when fossils were excluded, the combined analysis that included fossils recovered a monophyletic clade of Diapsida that excluded turtles. Lee’s (2001) study documents a dominance of morphological data coded for extant and fossil amniotes over the molecular data that were employed.

The soft anatomical characters employed by Lee (2001) in his combined analysis and their potential phylogenetic significance were scrutinized by Rieppel (2000a). The osteological characters and their coding used in the analyses of turtle relationships within amniotes (Lee, 1995, 1997a, 1997b; DeBraga & Rieppel, 1997; Rieppel & Reisz, 1999), in turn, were re-evaluated by Hill (2005), whose study is particularly important as it includes a broader taxon sampling than did previous studies and adds a suite (71) of new characters relating to the histology and osteological morphology of the integument and osteoderms. The significance of these added characters lies is the fact that they remove much of the ambiguity that was obtained when “the presence of dorsal dermal ossifications of any kind (trunk osteoderms or carapacial elements) [is interpreted] as a potential synapomorphy linking turtles with parareptiles” (Hill, 2005; compare also Lee, 1993, with Rieppel, 2001). On the basis of his data set, Hill (2005) obtained diapsid affinities of turtles again, yet in a novel tree topology that shows turtles to be the sister-group of lepidosaurs (Figure 13.1). This result reflects back on Broom’s (1924) comments on the striking similarities in the morphology of the pelvis and hind limbs that turtles share with Sphenodon (Rieppel, 1995).

On the whole, a general consensus seems to emerge that places turtles among the diapsid reptiles, but it remains to be seen whether they will be found to be more closely related to the lepidosauromorph or the archosauromorph clade among the Sauria. One possible reason for that remaining uncertainty may lie in the fact that the basal split of Sauria into a lepidosauromorph and an archosauromorph lineage is less well constrained than is currently acknowledged. However, most recently the occurrence of a cleithrum has been reported in the dermal pectoral girdle of the turtle Kayentachelys aprix from the Lower Jurassic of Arizona (Joyce et al., 2006). The cleithra identified in Kayentachelys and other basal fossil turtles such as Proganochelys and Proterochersys have alternatively been interpreted as dorsal epiplastral processes (Gaffney, 1990). Cleithra are reduced and lost early within reptiles, such that their presence in basal fossil turtles would conflict with a position of turtles among crown-group diapsids (Sauria) (Joyce et al., 2006).

The claim that a cleithrum is present in fossil basal turtles goes back to Jaekel’s (1915) description of the Upper Triassic turtle Stegochelys dux, now considered a junior synonym of Proganochelys quenstedti. Jaekel (1915) based his identification of a cleithrum in Proganochelys on its close

proximity to the upper end of the scapular process. But as noted by Gaffney (1990), the Berlin specimen of Proganochelys available to Jaekel (1915) did not preserve the anterior part of the plastron. Jaekel (1915) consequently did not recognize the cleithrum as a dorsal epiplastral process.

The homology of the epiplastron of turtles with the clavicle of other amniotes is undisputed (Jaekel, 1915; Zangerl, 1939, 1969; Gaffney, 1990; Joyce et al., 2006). Comparison of the pectoral girdle of Proganochelys with that of Captorhinus led Gaffney (1990) to homologize the dorsal epiplastral process of Proganochelys with the dorsal process of the clavicle in Captorhinus that is applied to the anterior edge of the scapular blade. To consider the dorsal epiplastral process a cleithrum would mean that the clavicle of fossil basal turtles lost all dorsal expansion as it was transformed into the epiplastron. The key feature used by Joyce et al. (2006) to claim the presence of a cleithrum in Kayentachelys is that some—but not all—of the specimens available appear to document a developmental origin of the dorsal epiplastral process that is independent from the epiplastron proper. The absence of sutures or sutural facets in Proganochelys, Proterochersis, and other specimens of Kayentachelys is claimed to document the ontogenetic fusion of the cleithrum with the epiplastron (clavicula). Given the nature of fossil material in general, and the frequent difficulty to distinguish sutures from breaks, the claim that a cleithrum is present in Kayentachelys, and by implication in other fossil basal turtles that have a dorsal epiplastral process, while not impossible, still appears ambiguous. In addition, the ontogenetic fusion of clavicle (epiplastron) and cleithrum would become a turtle synapomorphy, a condition unknown in any other tetrapod. But as noted by Joyce et al. (2006), the presence or absence of a cleithrum in basal turtles is but one character that is unlikely to reverse the signal of large-scale analyses. Whereas a lot still remains to be learned about the origin of turtles, their diapsid status seems to be the best supported hypothesis at this time.

13.4The Ecological Setting of Turtle Origins

The discussion of the ecological setting of turtle origins focuses on a terrestrial (Joyce & Gauthier, 2004) or, alternatively, an aquatic (Rieppel & Reisz, 1999) environment. The hypothesis of an aquatic origin of turtles was motivated by their possible sister-group relationship with sauropterygians, but because of ambiguous optimization of aquatic versus terrestrial habits on the cladogram, the argument was mostly based on physiological consideration. The development of the turtle shell did not only result in major morphological changes (Rieppel, 2001) but equally important physiological adaptations were required as well. Given that the ribs are embedded in the costal plates of the carapace, turtles had to evolve an entirely new mechanism for lung ventilation (Gaunt & Gans, 1969; Gans & Hughes, 1997). Respiration in turtles depends on volume changes of the tho- racico-peritoneal cavity inside the rigid dermal armor, which is achieved by altering the position of the limb flanks. Expansion of the thoracico-peritoneal cavity, supporting inhalation, involves the testocoracoideus muscle (Gaunt & Gans, 1969; Gans & Hughes, 1997), a probable homologue of the serratus ventralis muscle (Walker, 1971), which in other tetrapods suspends the pectoral girdle from the axial skeleton. The evolution of the turtle shell in terrestrial organisms would—in transitional stages—have resulted in conflicting functional roles for the muscle to play in locomotion and respiration. Because lung ventilation in aquatic turtles is not only supported by muscular activity but also, and to a significant degree, by hydrostatic pressure and gravity (Gaunt & Gans, 1969; Gans & Hughes, 1997), Rieppel and Reisz (1999) argued that the mechanisms of turtle respiration might have more plausibly evolved in an aquatic environment than on land. An aquatic origin of turtles might also be indicated by the function of the well-ossified turtle shell as an osmotic barrier (Bentley, 1976; see further discussion in Rieppel & Reisz, 1999). In contrast, Joyce and Gauthier (2004) found terrestrial and aquatic turtles to be characterized by different limb proportions, which indicate that the earliest and most basal fossil turtles—Proganochelys and Palaeochersys from the Upper Triassic of Germany and Argentina, respectively—were terrestrial. Their conclusion was that

turtles had a terrestrial origin but that terrestrial crown turtles are secondary land dwellers because crown turtles had an aquatic origin (Joyce, 2007).

The fossil record as presently known is unlikely to resolve the issue. Considered a terrestrial form by Joyce and Gauthier (2004), Proganochelys was considered to have been semi-aquatic (an aquatic bottom-walker) by Gaffney (1990). The earliest known unquestionable turtle carapace fragment (Joyce & Karl, 2006) comes from the Franconian Hauptmuschelkalk (Wild, 1972), which yielded the Bayreuth fauna that has been collected from a section of about 30 to 40 m belonging to the Trochitenkalk Formation and the lower part of the Meißner Formation (atavus through postspinosus biozone, Anisian, uppermost Illyrian; Hagdorn & Rieppel, 1999). As noted by Wild (1972) and Joyce and Karl (2006), the marine Bayreuth fauna includes allochtonous elements such as lungfish (Ceratodus) and labyrinthodont remains. Sedimentary markers (mica and find sand) indicate that these faunal elements may have been transported from the nearby Bohemian Massive not much more than 40 km away (Hagdorn & Rieppel, 1999). The possibility thus remains that Priscochelys hegnabrunnensis (Karl, 2005) is an allochtonous element of the marine Bayreuth fauna as well. However, whether this would imply fully terrestrial habits of Priscochelys remains open to debate (Hagdorn & Rieppel, 1999; Rieppel & Reisz, 1999). But because the turtle shell is already fully formed in Priscochelys, Proganochelys, Palaeochersys, and all other known fossil turtles, it is the missing intermediate forms that would have to be used in an attempt to further assess the ecological setting of turtle origins on the basis of the fossil record.

13.5Summary and Conclusions

Many of the questions that surround turtle origins remain unanswered at the present time. Whereas evidence for a diapsid status of turtles is accumulating, the precise relationships of turtles within diapsids remains a matter of debate and continued investigation. The ecological setting of turtle origins also remains open for further discussion. The difficulties encountered in research that addresses the origin of turtles no doubt originate from the highly modified body plan that characterizes the group and the absence of intermediate forms, either extant or fossil, that would offer some further clues as to how and where (under which conditions) the turtle body plan evolved. The ontogenetic development of the turtle carapace has become an important field of research for developmental biologists (Burke, 1989; Gilbert et al., 2001; Gilbert et al., 2004; Kuraku et al., 2005), but a link to a gradualistic model of turtle origination and evolution has not yet been successfully established (Rieppel, 2001).

Therefore, there is good reason to expect that ideas about turtle origins and evolution will continue to change. One of the evident directions to go is to pursue more comprehensive combined analyses, adding new data, both molecular and morphological, as they become available. Lee’s (2001) is so far the only combined analysis available, and whereas some of the osteological characters included in this analysis remain debatable, it could not include the integumentary characters offered by Hill (2005), nor did it include DNA data other than those offered by Zardoya and Meyer (1998). The other obvious source for further insight into turtle origins is the fossil record. New fossils, such as well-preserved Triassic procolophonids, could hold the potential to yet again turn the tables on turtle relationships—or better yet, fossils of intermediate structure could provide new clues to an understanding of the origin and evolution of the turtle body plan.

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