Patterns of Variation in the Phalangeal Formulae of Land Tortoises (Testudinidae): Developmental Constraint, Size, and Phylogenetic History CHARLES R
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JOURNAL OF EXPERIMENTAL ZOOLOGY (MOL DEV EVOL) 302B:134–146 (2004) Patterns of Variation in the Phalangeal Formulae of Land Tortoises (Testudinidae): Developmental Constraint, Size, and Phylogenetic History CHARLES R. CRUMLY1,w and MARCELO R. SA´NCHEZ-VILLAGRA2n 1Museum of Paleontology, University of California, Berkeley, California 94720 2Zoologisches Institut, Spezielle Zoologie, Universita¨t Tu¨bingen, Auf der Morgenstelle 28, D–72076 Tu¨bingen, Germany ABSTRACT Documentation of variation in phalangeal formulae in land tortoises combined with ontogenetic information from turtles in general were used, in a phylogenetic context, to infer the potential effect of size and developmental constraints upon patterns of morphological variation. A sample of 201 specimens and published illustrations of 37 tortoise species were examined, representing all but one living genera and most species of the Testudinidae. Specimens were either articulated dry skeletons or preserved animals that were x-rayed. The patterns of digital and phalangeal loss in tortoises were predicted from developmental studies of the manus and pes in other turtles. If a digit is lost, it is the first digit, which is the last one to develop. If a digit has a single phalanx, it is usually the fifth digit. The primitive phalangeal formula for land tortoises is probably 2–2–2–2–1, the most common pattern found in living testudinid species. The presence of a second phalanx in the fifth digit evolved independently many times and usually in large tortoises. Such additions were interpreted as instances of peramorphosis. Many small tortoises have a full complement of digits (five) and phalanges (two in each digit); nevertheless, phalangeal and digital loss is associated with small size. Small and medium size tortoises exhibit greater variation in phalangeal number than do large tortoises. We hypothesize that epigenetic processes, and not simply adaptation, played a major role in the evolution of the variation in phalangeal formulae in tortoises. J. Exp. Zool. (Mol. Dev. Evol.) 302B:134–146, 2004. r 2004 Wiley-Liss, Inc. INTRODUCTION turtles that includes numerous fossil and living taxa and a wide variation in size (Auffenberg, ’74; Manus and pes are convenient character com- Ernst and Barbour, ’89). Documentation of varia- plexes in studies of ontogeny and phylogeny tion in phalangeal formulae in land tortoises because the various phenotypes are discrete and combined with ontogenetic information from the product of similar developmental processes turtles in general are used here, in a phylogenetic shared by most tetrapods (Schmalhausen, ’15; context, to infer the potential effect of size Sewertzoff, ’31; Shubin and Alberch, ’86). The and developmental constraints upon patterns of potential relation of these developmental pro- morphological variation. cesses and constraints to phalangeal reduction in amniotes has been recently reviewed by Richard- son and Chipman (2003). Grant sponsors: NSF; Grant number: DEB 8114467; Smithsonian The manus and pes of turtles are character Predoctoral Fellowship; Deutscher Akademischer Austauschdienst; complexes that experienced numerous trans- Ernst Mayr Fund of the Museum of Comparative Zoology, American Philosophical Society; NSF; Grant number: BSR 8407437 to P. formations during their evolution, including Alberch (CRC). reduction in some of the most basal stem repre- This is UCMP contribution 1849. wDr. Crumly’s mailing address: University of California Press, sentatives, modifications of the flippers of Science Publishing Group, 2120 Berkeley Way, Berkeley, CA 94704- marine turtles, and supernumerary phalanges 1012. E-mail: [email protected] nCorrespondence to: Marcelo R. Sa´nchez-Villagra, Department of in some soft-shell turtles (Rabl, ’10; Walker, ’73; Palaeontology, Natural History Museum, Cromwell Road, London Gaffney, ’90; Meylan, ’96; Sheil, 2003; Rougier SW7 5BD, UK. E-mail: [email protected] Received 8 October 2003; Accepted 29 January 2004 et al., ’98;). Of particular interest are land Published online in Wiley InterScience (www.interscience.wiley. tortoises (Testudinidae), a diverse clade of living com). 10.1002/jez.b.20010 r 2004 WILEY-LISS, INC. PHALANGEAL FORMULAE IN TORTOISES 135 The understanding of phalangeal formula evo- pre-requisite to the development of other subse- lution in reptiles (Greer, ’91) has greatly benefited quent elements. This hierarchy of events implies from consideration of comparative data and that terminal events in a sequence are expected development at lower taxonomic levels (Shapiro, to be lost in evolution more easily than more 2002; Shapiro et al., 2003), rather than compar- basal elements. This principle is expected to isons among model organisms. generate non-random patterns of homoplasy and Studies of the ontogeny of limbs in selected synapomorphy in the phylogeny of the tortoise tetrapods (Essex, ’27; Gans, ’75; Holder, ’83; autopodials. Hinchliffe, ’85; Crumly, ’90; Mu¨ller, ’91; Goodwin Size is another factor that can affect morpholo- and Trainor, ’83; Oster et al., ’85; Buscalioni gical outcome in autopodial development. If et al., ’97; Larsson and Wagner, 2002; Richardson chondrogenesis of an element is dependent on a and Oelschla¨ger, 2002) have offered insights critical minimum number of mesenchymal cells, and predictions about the pattern of digital and reduction in size can lead to reduction in number phalangeal loss and gain, in most cases under the of elements (e.g., Alberch and Gale, ’83, p. 193). assumption that changes in phenotype are the result of heterochronic shifts (Richardson and Evolution and development of manus and Chipman, 2003). pes in turtles In this context, recognition of the processess involved in the formation of cartilaginous limb Burke and Alberch (’85) demonstrated that the elements and the digital arch and primary axis developmental pattern of the manus and pes of (Shubin and Alberch, ’86) have been of funda- frogs and some turtles (Chrysemys picta and mental importance. Shubin and Alberch (’86) Chelydra serpentina, see Table 1 and Fig. 1) is identified ontogenetically dynamic processes that similar. However, there are minor differences result in three patterns of connectivity in the between anuran and chelonian manus and pes formation of cartilagenous limb elements in tetra- ontogeny. Concerning the manus of frogs, for pods. A mesenchymal chondrogenetic element example, the earliest digit to develop is the fourth may form without connectivity, usually near the followed closely by the third digit (fide Shubin and beginning of the process of limb formation (e.g., in Alberch, ’86), and then synchronously by the the formation of the humerus or femur). A second second and fifth digits, and finally the first digit. alternative is that a single element branches The fifth digit is a de novo unconnected structure, resulting in two elements distal to the division. i.e. it shows no embryonic affiliations to more This process is called bifurcation (apparently proximal elements of the manus. In contrast to trifurcations or other polychotomies are never this, among turtles the fourth digit develops well observed, perhaps for the reasons suggested by before the third, not at the same time. Further- Oster and Alberch, ’82). Last, a single mesenchy- more, the fifth digit forms synchronously with the mal condensation may either bud off a new third digit, rather than the second digit as in frogs. condensation distally or become subdivided into There are only a few studies of the ontogeny of two separate elements. This last process is called the manus of turtles besides that of Burke and segmentation. There is a conserved sequence Alberch (’85). Rosenberg (1892) described the in which these processess occur in the ontogeny ontogeny of the manus of Emys orbicularis. Baur of the turtle autopodials (primary axis, digital (1892) re-interpreted the homologies suggested by arch), so that the appearance of some elements is a Rosenberg‘s results, and Burke and Alberch (’85) TABLE 1. Di¡erences between urodelian, anuran and chelonian digital development (taken from Alberch and Gale,’85, and Shubin and Alberch,’86) Chelydra serpentina and Salamanders Frogs Chrysemys picta I and II di¡erentiate ¢rst IV di¡erentiates ¢rst IV di¡erentiates ¢rst III and IV di¡erentiate sequentially (asynchronously) II and V di¡erentiate next III and V di¡erentiate next (synchronously) (synchronously) digits di¡erentiate in a post-axial direction digits di¡erentiate in a digits di¡erentiate in a pre-axial direction pre-axial direction 136 C. R. CRUMLY AND M. R. SA´NCHEZ-VILLAGRA Fig. 1. A diagramatic summary of the development of the ontogeny. Abbreviations: I-V metacarpals 1 through 5, c 1–5 carpus in Chrysemys picta and Chelydra serpentina (taken distal carpals 1–5, cl-cm centrale, p pisiform, R radius, from Burke and Alberch, ’85). The adult morphology of land u ulnare, U ulna. tortoises suggests that they develop by means of a similar supported Baur‘s interpretation. The sequence of turtles. He noted that tortoises have four clawed chondrification and ossification in the hand of digits, which have two phalanges each, and some- some turtle species were described and discussed times a fifth invisible unclawed digit that that has by Rieppel (’93, Chelydra serpentina) and by Sheil a single phalanx. Only four species of land (2003, Apalone spinifera). tortoises were examined by Zug: Geochelone sp., Auffenberg (’66) examined the adult carpus of Gopherus berlandieri, G. Polyphemus, and Kinixys several