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Dissociation of Somatic Growth from Segmentation Drives Gigantism In Biol. Lett. (2007) 3, 296–298 Gigantism (Gould & McFadden 2004, p. 220)is doi:10.1098/rsbl.2007.0069 pronounced in boids, pythonids and typhlopids Published online 27 March 2007 among snakes (Greene 1997; Murphy & Henderson Evolutionary developmental biology 1997; Kley 2003). The largest extant snakes consist of the pythonids, Python molurus, Python sebae (incl. natalensis), and Python reticulatus and the boid Dissociation of somatic Eunectes murinus (green anaconda), with reliable maximum body lengths between 7 and 9 m (Murphy & growth from segmentation Henderson 1997). The typhlopid genera Ty p h l o p s and Rhinotyphlops include some of the smallest snake drives gigantism in snakes species (total body length; TBL approx. 10 cm) as well as comparative giants including Typhlops 1,* 2 Jason J. Head and P. David Polly punctatus, Typhlops angolensis, Typhlops lineolatus and 1 Department of Biology, University of Toronto at Mississauga, Rhinotyphlops schlegelii, which achieve body lengths 3359 Mississauga Road N., Mississauga, Ontario L5L1C6, Canada 2Department of Geological Sciences, Indiana University, approaching 1 m (Roux-Este`ve 1974; Kley 2003). 1001 E 10th Street, Bloomington, IN 47405-1405, USA Here, we test developmental mechanisms under- *Author for correspondence ( [email protected]). lying the evolution of gigantism by examining the Body size is significantly correlated with num- relationship between body size and vertebral numbers ber of vertebrae (pleomerism) in multiple among the largest and the smallest snakes. If pleomer- vertebrate lineages, indicating that change in ism is the primary mechanism of body size evolution in number of body segments produced during snakes, then body size and axial segment counts should somitogenesis is an important factor in covary, but if other mechanisms, such as regulation of evolutionary change in body size, but the role of somatic growth, are responsible for body size evolution, segmentation in the evolution of extreme sizes, then size and segment number will be unrelated. including gigantism, has not been examined. We explored the relationship between body size and vertebral count in basal snakes that exhibit 2. MATERIAL AND METHODS gigantism. Boids, pythonids and the typhlopid Body size measurements and vertebral counts were collected from genera, Typhlops and Rhinotyphlops, possess a examination of museum osteological collections and the literature (see positive relationship between body size and electronic supplementary material). Body size was measured as snout- vent length (SVL) in Boidae (Boinae, Ungaliophiinae and Erycinae; vertebral count, confirming the importance of Lawson et al.2004; Burbrink 2005) and Pythonidae, and vertebral pleomerism; however, giant taxa possessed counts represent precloacal elements. Typhlops and Rhinotyphlops fewer than expected vertebrae, indicating that a possess extremely abbreviated tails representing approximately 1% of separate process underlies the evolution of TBL (Kley 2003). As a result, TBL approximates SVL in these taxa, gigantism in snakes. The lack of correlation and was compared to maximum total number of vertebrae (Roux- between body size and vertebral number in Este`ve 1974). No SVL statistics are published for the largest individuals of Eunectes and Python, so we estimated those by taking giant taxa demonstrates dissociation of segment TBL for the largest verifiable published specimens (Murphy & production in early development from somatic Henderson 1997) and multiplying by the proportion of SVL/TBL growth during maturation, indicating that derived from data on smaller individuals of Eunectes notaeus (Dirksen gigantism is achieved by modifying development 2002)andPython (Shine et al.1998). at a different stage from that normally selected Ventral scale counts correlate with vertebral numbers in most for changes in body size. alethinophidian snakes (Alexander & Gans 1966) and are com- monly used as proxy data for vertebral counts (Lindell 1994; Shine Keywords: gigantism; pleomerism; somitogenesis; 2000). We used scale counts where skeletal material and vertebral dissociation; heterochrony; snakes counts were not available, and used the average of male and female counts for boids and pythonids because sex data were often not available for either specimens or the literature, despite strong dimorphism in vertebral numbers and body lengths for many taxa (e.g. Shine 2000). 1. INTRODUCTION We used phylogenetic generalized least squares regression Extrinsic selective factors influencing the evolution of (PGLS; Martins & Hansen 1997) to determine the relationship of body size to vertebral numbers while taking into account the effects body size extremes in vertebrates have been heavily of phylogenetic autocorrelation, with body size as the dependent studied (Hanken & Wake 1993; Alexander 1998), but variable regressed onto independent vertebral counts using the intrinsic developmental mechanisms underlying COMPARE v. 4.6b (Martins 2004). We incorporated phylogenetic evolutionary body size change are poorly known. topologies derived from molecular and morphological datasets (electronic supplementary material). Resolved branch lengths were Phyletic body size increases are associated with set to 1.0. Unresolved polytomies were artificially resolved with increased somite numbers (pleomerism) in actinop- branch lengths of 0.001 to satisfy the algorithmic requirements of terygian fish (Lindsey 1975), plethodontid salaman- COMPARE. The small length of unresolved branches is effectively zero as far as the results are concerned (Martins & Hansen 1997). ders (Jockusch 1997) and derived colubroid snakes (Lindell 1994), but not in groups whose vertebral column is highly regionalized and functionally con- 3. RESULTS strained like mammals and birds (Wake 1979), in Phylogenetic generalized least squares regression pro- which body size changes are a function of post- duced a positive and significant correlation in Boidae embryonic somatic growth. Although pleomerism has (rZ0.46, p!0.01), Pythonidae (rZ0.38, pZ0.03) Z Z been established as a mechanism of body size and Ty p h l o p s (r 0.41, p 0.03; figure 1). Rhinotyphlops evolution in snakes, its role in the evolution of possessed positive but non-significant correlations Z Z gigantism is unknown. (Rhinotyphlops: r 0.31, p 0.12), resulting from extremely low vertebral numbers in the largest taxa. Electronic supplementary material is available at http://dx.doi.org/ Excluding giants from the regressions increased the 10.1098/rsbl.2007.0069 or via http://www.journals.royalsoc.ac.uk. positive relationships between vertebral counts and Received 5 February 2007 296 This journal is q 2007 The Royal Society Accepted 22 February 2007 Gigantism and development in snakes J. J. Head & P. D. Polly 297 (a) 8000 (b) 900 Boidae Typhlops 7000 Pythonidae 800 Rhinotyphlops 6000 700 600 5000 500 4000 400 3000 300 total length (mm) 2000 snout–vent length (mm) 200 1000 100 0 0 100 150 200 250 300 350 400 450 500 100 150 200 250 300 350 400 450 500 vertebrae vertebrae Figure 1. Average vertebral counts plotted against maximum body length for (a) Boidae and Pythonidae and (b) typhlopids. Overlain trend lines are PGLS regressions omitting giant taxa. Dashed lines represent (a) Boidae and (b) Typhlops. PGLS Regression equations (omitting giant taxa) are: Boidae, yZ11.29xK1202.2; Pythonidae, yZ9.25xK628.2; Ty p h l o p s , yZ1.95xK157.2; Rhinotyphlops, yZ0.89xC89.8. Squares represent giant taxa. body size in all clades (Boidae: rZ0.50, p!0.01; Giant taxa possess relatively low numbers of Pythonidae: rZ0.71, p!0.01; Typhlops: rZ0.63, vertebrae indicating that pleomerism is not the p!0.01; Rhinotyphlops: rZ0.70, p!0.01). The largest primary mechanism underlying attainment of excep- species in all four clades have fewer than the expected tionally large body size. Pleomerism is a phenomenon precloacal vertebrae (figure 1). The largest boids, associated with segmentation and somitogenesis in pythonids and Typhlops have vertebral counts near the the early stages of embryogenesis, but the large size mean for their respective clades, and the R. schlegelii attained by giant snakes must be due to modification complex possessed among the lowest counts in the of post-somitogenetic somatic growth. Normally, in genus. snakes somite number and post-embryonic growth are closely associated, but in giant species these two developmental processes are dissociated (sensu 4. DISCUSSION Results of this study demonstrate pleomerism in basal Raff 1996). taxa, indicating that the phenomenon occurs through- With the exception of three viperid taxa (Lindell out snake phylogeny. Snakes have a greater variability 1994, fig. 11F ), dissociation does not appear to play in vertebral numbers than do other amniotes, aroleinattainmentofmaximumbodysizesin probably resulting from developmental homogeniz- derived colubroid snakes. Colubroids do not achieve ation of the axial skeleton. In snakes, axial regionali- the extreme absolute sizes or magnitude of size range zation is reduced by anterior expansion of expression in boids and pythonids, but do achieve the sizes and domains for Hox genes that code for the dorsal region ranges in examined typhlopids. The absence of of the vertebral column, suppressing expression of a dissociation in the majority of examined derived taxa distinct cervical region (Cohn & Tickle 1999). As a may represent greater constraint on somatic growth result, normal constraints on vertebral numbers may relative to basal snakes. be released,
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