Repeated Origin and Loss of Adhesive Toepads in Geckos

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Repeated Origin and Loss of Adhesive Toepads in Geckos Marquette University e-Publications@Marquette Biological Sciences Faculty Research and Publications Biological Sciences, Department of 6-27-2012 Repeated Origin and Loss of Adhesive Toepads in Geckos Tony Gamble Eli Greenbaum Todd R. Jackman Anthony P. Russell Aaron M. Bauer Follow this and additional works at: https://epublications.marquette.edu/bio_fac Part of the Biology Commons Repeated Origin and Loss of Adhesive Toepads in Geckos Tony Gamble1,2, Eli Greenbaum3¤, Todd R. Jackman3, Anthony P. Russell4, Aaron M. Bauer3* 1 Department of Genetics, Cell Biology and Development, University of Minnesota, Minneapolis, Minnesota, United States of America, 2 Bell Museum of Natural History, University of Minnesota, St. Paul, Minnesota, United States of America, 3 Department of Biology, Villanova University, Villanova, Pennsylvania, United States of America, 4 Department of Biological Sciences, University Department of Calgary, Calgary, Canada Abstract Geckos are well known for their extraordinary clinging abilities and many species easily scale vertical or even inverted surfaces. This ability is enabled by a complex digital adhesive mechanism (adhesive toepads) that employs van der Waals based adhesion, augmented by frictional forces. Numerous morphological traits and behaviors have evolved to facilitate deployment of the adhesive mechanism, maximize adhesive force and enable release from the substrate. The complex digital morphologies that result allow geckos to interact with their environment in a novel fashion quite differently from most other lizards. Details of toepad morphology suggest multiple gains and losses of the adhesive mechanism, but lack of a comprehensive phylogeny has hindered efforts to determine how frequently adhesive toepads have been gained and lost. Here we present a multigene phylogeny of geckos, including 107 of 118 recognized genera, and determine that adhesive toepads have been gained and lost multiple times, and remarkably, with approximately equal frequency. The most likely hypothesis suggests that adhesive toepads evolved 11 times and were lost nine times. The overall external morphology of the toepad is strikingly similar in many lineages in which it is independently derived, but lineage-specific differences are evident, particularly regarding internal anatomy, with unique morphological patterns defining each independent derivation. Citation: Gamble T, Greenbaum E, Jackman TR, Russell AP, Bauer AM (2012) Repeated Origin and Loss of Adhesive Toepads in Geckos. PLoS ONE 7(6): e39429. doi:10.1371/journal.pone.0039429 Editor: Jose Castresana, Institute of Evolutionary Biology (CSIC-UPF), Spain Received January 17, 2012; Accepted May 23, 2012; Published June 27, 2012 Copyright: ß 2012 Gamble et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This research was supported by grants DEB 0515909 and DEB 0844523 from the National science Foundation (www.nsf.gov) and by Discovery Grant 9745-2008 from the Natural Sciences and Engineering Research Council of Canada (www.nserc-crsng.gc.ca). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] ¤ Current address: Department of Biological Sciences, University of Texas at El Paso, El Paso, Texas, United States of America Introduction which promote adhesion via van der Waals forces and complex frictional interactions [12,13,14,15]. Setae evolved from the Repeated evolution, also called convergent or parallel evolution, microscopic spinules that are typical of the outer epidermis of all is the independent emergence of similar traits in separate limbed gekkotans and some other squamates [15,16,17,18], and evolutionary lineages and is typically seen as evidence of are hypothesized to aid in skin shedding [16,19]. A hierarchy of adaptation through natural selection or of developmental con- anatomical specializations have evolved to govern the adhesive straints that limit or bias morphological evolution [1,2,3,4,5]. properties of the setae, and dynamic interactions with the substrate Examining instances of repeated evolution serves as an important depend on numerous morphological adaptations and behaviors means of studying evolutionary processes and is analogous to that facilitate control of the adhesive mechanism during locomo- studying multiple experimental replicates [6]. Indeed, each case of tion [13,20,21,22,23]. Collectively, these specializations permit convergent or parallel evolution reveals the degree of common effective and rapid application and removal of the setae with response to some fundamental biological challenge. As a result, reference to the substrate and constitute a functionally integrated extensive effort has been devoted to identifying instances of complex [13,24]. repeated evolution. To do this effectively, an accurate phylogeny is Geckos are among the most species-rich and geographically required for the ‘‘mapping’’ of traits and to permit examination of widespread of terrestrial vertebrate lineages, with ,1450 described whether similarity is the result of shared ancestry or represents true species in 118 genera, and comprise 25% of all described lizard independent derivation [3]. Many aspects of vertebrate body form species [25]. They are the likely sister group of all other lizards and related to locomotion have evolved repeatedly, being both gained snakes, excluding the limbless dibamids, having diverged from and lost many times over. This includes functionally significant other squamates 225–180 MY ago [26,27]. The gekkotan adhesive traits such as wings as aerodynamic devices, and limb reduction or system has been present since at least the mid-Cretaceous, as elimination associated with burrowing [7,8,9]. Likewise, adhesive revealed by scansorial pads preserved in amber-embedded gecko toepads employed in climbing have evolved several times in fossils [28,29]. Approximately 60% of gecko species possess vertebrates, including multiple lineages of treefrogs, Anolis lizards, adhesive toepads, whereas the remainder lack functional adhesive Prasinohaema skinks and, perhaps most notably in geckos [10,11]. toepads (or lack limbs altogether, in the case of the Australian The key component of the adhesive apparatus in lizards is the pygopodid geckos) [7]. Geckos with adhesive toepads can easily presence of setae, microscopic hair-like outgrowths of the scale vertical or even inverted surfaces, and these extraordinary superficial layer of the subdigital epidermis (the Oberha¨utchen), clinging abilities have long attracted scientific attention [16,30,31]. PLoS ONE | www.plosone.org 1 June 2012 | Volume 7 | Issue 6 | e39429 Origin and Loss of Adhesive Toepads in Geckos Recently, interest has focused on mimicking the gecko adhesive for tRNAs. This partitioning scheme contains fewer parameters mechanism to develop bio-inspired technologies [32,33,34]. Bio- than the preferred partitioning strategy used in previous phyloge- mimetic studies have concentrated largely on adhesion at the netic analyses of the same nuclear loci (partitioning by both gene molecular level, but functional control of adhesive toepads requires and codon), but with far fewer taxa [43,49]. The more parameter- integration across a hierarchy of systems operating at different rich strategy resulted in convergence problems in the Bayesian scales. These complex interactions – from molecular bonds to the analysis of this taxon-rich dataset, likely due to low phylogenetic locomotor control of the entire organism – are incorporated across signal in the smaller partitions; these problems were resolved by seven orders of magnitude of size in geckos [13]. reducing the number of partitions. Model selection was based on The form and structure of adhesive toepads in geckos have been AIC scores using the software jModeltest [50], which recovered used historically for taxonomic purposes, chiefly for assigning either the GTR + I + G or the GTR + G models for each partition species to genera [35,36,37]. Traditional views of gecko evolution (Table S2). The GTR + G model was used for all partitions in the presupposed a single [38], or at most two [22], origins of the ML analysis, which is the only model implemented in RAxML due adhesive apparatus. These views were inferred from phylogenetic to problematic interactions between the I and G parameters hypotheses that used few characters and sparse taxon sampling, [51,52]. Bayesian analyses were run with multiple MCMC chains and that placed the padless eublepharid geckos as sister to all for 40 million generations, sampling every 1000th generation. Post remaining geckos, a position refuted by recent molecular burn-in convergence was checked by visual inspection of likelihood phylogenies [26,27,39,40]. Reconstructing the evolution of values by generation using Tracer 1.5 [53] and comparing split gekkotan adhesive toepads, therefore, requires a comprehensive frequencies between runs using AWTY [54]. phylogeny derived from an independent data source, i.e., molecular genetic data. Here we estimate the phylogenetic Comparative Analyses relationships among nearly all recognized gecko genera using We categorized digital morphologies in all sampled taxa as a multilocus dataset. We
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