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Integrative and Comparative Biology Integrative and Comparative Biology, Volume 60, Number 1, Pp Integrative and Comparative Biology Integrative and Comparative Biology, volume 60, number 1, pp. 190–201 doi:10.1093/icb/icaa015 Society for Integrative and Comparative Biology SYMPOSIUM Convergent Evolution of Elongate Forms in Craniates and of Locomotion in Elongate Squamate Reptiles Downloaded from https://academic.oup.com/icb/article-abstract/60/1/190/5813730 by Clark University user on 24 July 2020 Philip J. Bergmann ,* Sara D. W. Mann,* Gen Morinaga,1,*,† Elyse S. Freitas‡ and Cameron D. Siler‡ *Department of Biology, Clark University, Worcester, MA, USA; †Department of Integrative Biology, Oklahoma State University, Stillwater, OK, USA; ‡Department of Biology and Sam Noble Oklahoma Museum of Natural History, University of Oklahoma, Norman, OK, USA From the symposium “Long Limbless Locomotors: The Mechanics and Biology of Elongate, Limbless Vertebrate Locomotion” presented at the annual meeting of the Society for Integrative and Comparative Biology January 3–7, 2020 at Austin, Texas. 1E-mail: [email protected] Synopsis Elongate, snake- or eel-like, body forms have evolved convergently many times in most major lineages of vertebrates. Despite studies of various clades with elongate species, we still lack an understanding of their evolutionary dynamics and distribution on the vertebrate tree of life. We also do not know whether this convergence in body form coincides with convergence at other biological levels. Here, we present the first craniate-wide analysis of how many times elongate body forms have evolved, as well as rates of its evolution and reversion to a non-elongate form. We then focus on five convergently elongate squamate species and test if they converged in vertebral number and shape, as well as their locomotor performance and kinematics. We compared each elongate species to closely related quadrupedal species and determined whether the direction of vertebral or locomotor change matched in each case. The five lineages examined are obscure species from remote locations, providing a valuable glimpse into their biology. They are the skink lizards Brachymeles lukbani, Lerista praepedita, and Isopachys anguinoides, the basal squamate Dibamus novaeguineae, and the basal snake Malayotyphlops cf. ruficaudus. Our results support convergence among these species in the number of trunk and caudal vertebrae, but not vertebral shape. We also find that the elongate species are relatively slower than their limbed counterparts and move with lower frequency and higher amplitude body undulations, with the exception of Isopachys. This is among the first evidence of locomotor convergence across distantly related, elongate species. Introduction Published work shows that elongate forms may Elongate forms have evolved many times in most have evolved differently across vertebrate clades. major lineages of vertebrates (Lande 1978; Greer For example, in fishes, elongation can occur through 1991; Caldwell 2003; Wiens et al. 2006; Brandley elongation of the head, trunk, or tail, and by addi- et al. 2008; Ward and Mehta 2014; Law et al. tion and/or lengthening of vertebrae (Ward and 2019). Therefore, their convergent evolution is a ma- Brainerd 2007; Ward and Mehta 2014). jor theme in vertebrate evolution. However, despite Salamanders evolve body elongation through the much study of some focal clades of elongate species, lengthening of the trunk and tail and by either ad- their evolutionary distribution across vertebrates, dition or elongation of the vertebrae (Parra-Olea and and whether these independent instances are devel- Wake 2001; Wake et al. 2011). In contrast, body opmentally (Infante et al. 2018; Leal and Cohn elongation in squamates (lizards and snakes) occurs 2018), functionally (Bergmann and Irschick 2010; through the addition of vertebrae and the lengthen- Barros et al. 2011), and ecologically convergent ing of the body or both the body and tail (Bergmann (Kendrick 1991; Grizante et al. 2012) remains poorly and Irschick 2012; Wiens et al. 2006; Brandley et al. understood. 2008; Bergmann and Morinaga 2019). Finally, in Advance Access publication March 30, 2020 ß The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. Convergence in snake-like lizards 191 mustelids and whales, the regional lengthening of locomotor performance and kinematics in five focal trunk vertebrae is responsible for elongation of the examples of convergently elongate squamate species. body rather than increasing the number of vertebrae Our five elongate species represent obscure and (Buchholtz 2001; Law et al. 2019). understudied taxa that live in relatively remote loca- Understanding the evolution of locomotion in tions: Lerista praepedita from Australia, Brachymeles elongate forms also remains poorly understood. lukbani, Dibamus anguinoides, and Malayotyphlops cf. The transition from quadrupedal to elongate and ruficaudus from the Philippines, and Isopachys angui- limb-reduced form involves a transition from limb- noides from Thailand. These five examples have based to axial propulsion by body undulation (Gans evolved independently, sharing most recent common Downloaded from https://academic.oup.com/icb/article-abstract/60/1/190/5813730 by Clark University user on 24 July 2020 1986; Renous et al. 1998). This seems obvious, yet ancestor’s 45–205 mya (Zheng and Wiens 2016). transitional forms use limb and axial propulsion si- multaneously (Gans and Fusari 1994; Renous et al. Methods 1999; Bergmann and Irschick 2010), and sprawling quadrupeds also undulate their bodies (Renous et al. Phylogeny and elongation data collection and 1995; Renous et al. 1998). Some evidence suggests analysis that elongate forms with reduced or absent limbs We quantified the number of times elongate body undulate their bodies at lower frequencies and rela- forms evolved across the Craniata using evolutionary tively larger amplitudes than quadrupedal forms Markov models. We used a published family-level (Gans and Fusari 1994; Renous et al. 1999; tree of all life (Scholl and Wiens 2016) and edited Morinaga and Bergmann 2019). However, it remains it in R v3.6.1 (R Core Team 2019) with the “geiger” unknown whether convergent elongate limbless (Pennell et al. 2014) and “phytools” (Revell 2012) forms have also convergently evolved their locomo- packages. We pruned the phylogeny to include tion relative to their limbed relatives. only vertebrates, manually added the Polypteridae The evolution of elongate body forms is also re- as sister to the other ray-finned fishes (Rabosky lated to various ecological variables. For example, et al. 2018) and combined our vertebrate phylogeny gymnophthalmid lizards that inhabit looser soil with that of the Agnatha (Kuraku and Kuratani have longer, more tapering snouts and are more 2006), resulting in a phylogeny of 783 families. elongate with smaller limbs (Barros et al. 2011; Only nine nodes were unresolved, so we resolved Grizante et al. 2012). Australian Lerista species that them arbitrarily and set their branch lengths equal are more snake-like tend to have smaller range sizes, to 0.01 million years. We made small adjustments to possibly due to lower dispersal abilities (Lee et al. branch lengths to ensure ultrametry by minimizing 2013). In lizards, elongate limbless forms that live sum of square differences between non-ultrametric in cluttered habitats tend to have long tails, while and ultrametric trees (Revell 2012). fossorial species tend to have shorter tails (Wiens We discretely categorized each family as either et al. 2006). However, fossorial elongate lizards live having evolved one or more elongate species or not in a wide diversity of habitats from arid deserts with by surveying the elongation literature (cited in loose sand substrates to wet tropical forests with “Introduction” section), and qualitatively surveying packed, water-saturated soil (Kendrick 1991; online resources. We did the latter by searching for Branch 1998; Siler et al. 2011; Grizante et al. each family using Google and observing a range of 2012). These differences in habitat suggest that con- images for each. We vetted sources to ensure that vergently elongate taxa may need to adopt divergent observed images represented the identified clades. locomotor strategies to negotiate their respective Then a visual determination of whether observed habitats. species were elongate was made. Any borderline phe- Here, we set the context for the study of elongate notypes were considered not elongate. While this ap- body forms by surveying their evolutionary distribu- proach is not quantitative, most examples were tion among vertebrates, and then focus on five con- obvious, and our intent was to provide a compre- vergently elongate squamate species to test for hensive starting point to spur research in previously convergent evolution of their locomotion. First, we overlooked clades. These data (Supplementary Table survey the distribution of elongate bodies in crani- S1) and the phylogeny are available in ates (vertebrates and their sister group, the Agnatha). Supplementary Material. We provide a catalog of clades in which this body We modeled the evolution of elongation in crani- form has evolved, determine how many times it has ates by fitting two discrete Markov models to the evolved, and quantify its likelihood of being ances- data with likelihood (Schluter et al. 1997 ) using tral. Second, we test for convergence of surface
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