in

Evolution of the locomotor skeleton in Anolis lizards reflects the interplay between ecological opportunity and phylogenetic inertia

[adace-ad id="91168"]
  • 1.

    Grant, P. R. & Grant, B. R. How and why Species Multiply: The Radiation of Darwin’s Finches. (Princeton University Press, 2008).

  • 2.

    Baldwin, B. G. & Sanderson, M. J. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proc. Natl Acad. Sci. USA 95, 9402–9406 (1998).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 3.

    Losos, J. B. & Ricklefs, R. E. Adaptation and diversification on islands. Nature 457, 830–836 (2009).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 4.

    Macarthur, R. H. & Wilson, E. O. The Theory of Island Biogeography. (Princeton University Press, 1967).

  • 5.

    Lewontin, R. C. The organism as the subject and object of evolution. Scientia 77, 65 (1983).

    Google Scholar 

  • 6.

    Blows, M. W. & Hoffmann, A. A. A reassessment of genetic limits to evolutionary change. Ecology 86, 1371–1384 (2005).

    Article  Google Scholar 

  • 7.

    Hansen, T. F. & Houle, D. Measuring and comparing evolvability and constraint in multivariate characters. J. Evol. Biol. 21, 1201–1219 (2008).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 8.

    West-Eberhard, M. J. Developmental Plasticity and Evolution. (Oxford University Press, 2003).

  • 9.

    Wagner, G. P. & Altenberg, L. Perspective: complex adaptations and the evolution of evolvability. Evolution 50, 967–976 (1996).

    PubMed  Article  PubMed Central  Google Scholar 

  • 10.

    Hendrikse, J. L., Parsons, T. E. & Hallgrímsson, B. Evolvability as the proper focus of evolutionary developmental biology. Evol. Dev. 9, 393–401 (2007).

    PubMed  Article  PubMed Central  Google Scholar 

  • 11.

    Klingenberg, C. P. Studying morphological integration and modularity at multiple levels: concepts and analysis. Philos. Trans. R. Soc. B 369, 20130249 (2014).

    Article  Google Scholar 

  • 12.

    Jablonski, D. Approaches to macroevolution: 1. General concepts and origin of variation. Evol. Biol. 44, 427–450 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  • 13.

    Uller, T., Moczek, A. P., Watson, R. A., Brakefield, P. M. & Laland, K. N. Developmental bias and evolution: a regulatory network perspective. Genetics 209, 949–966 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 14.

    Hansen, T. F. Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability. Biosystems 69, 83–94 (2003).

    PubMed  Article  PubMed Central  Google Scholar 

  • 15.

    Goswami, A., Binder, W. J., Meachen, J. & O’Keefe, F. R. The fossil record of phenotypic and modularity: a deep-time perspective on developmental and evolutionary dynamics. Proc. Natl Acad. Sci. USA 112, 4891–4896 (2015).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 16.

    Armbruster, W. S., Pelabon, C., Bolstad, G. H. & Hansen, T. F. Integrated phenotypes: understanding trait covariation in plants and animals. Philos. Trans. R. Soc. B 369, 20130245 (2014).

    Article  Google Scholar 

  • 17.

    Felice, R. N., Randau, M. & Goswami, A. A fly in a tube: macroevolutionary expectations for integrated phenotypes. Evolution 72, 2580–2594 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 18.

    Goswami, A., Smaers, J. B., Soligo, C. & Polly, P. D. The macroevolutionary consequences of phenotypic integration: from development to deep time. Philos. Trans. R. Soc. B 369, 20130254 (2014).

    CAS  Article  Google Scholar 

  • 19.

    Cheverud, J. M. Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution 36, 499–516 (1982).

    PubMed  Article  PubMed Central  Google Scholar 

  • 20.

    Wagner, G. P., Pavlicev, M. & Cheverud, J. M. The road to modularity. Nat. Rev. Genet. 8, 921–931 (2007).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 21.

    Melo, D., Porto, A., Cheverud, J. M. & Marroig, G. Modularity: genes, development and evolution. Annu. Rev. Ecol. Evol. Syst. 47, 463–486 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  • 22.

    Gerhart, J. & Kirschner, M. The theory of facilitated variation. Proc. Natl Acad. Sci. USA 104, 8582–8589 (2007).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 23.

    Villmoare, B., Fish, J. & Jungers, W. Selection, morphological integration, and strepsirrhine locomotor adaptations. Evol. Biol. 38, 88–99 (2011).

    Article  Google Scholar 

  • 24.

    Navalon, G., Marugan-Lobon, J., Bright, J. A., Cooney, C. R. & Rayfield, E. J. The consequences of craniofacial integration for the adaptive radiations of Darwin’s finches and Hawaiian honeycreepers. Nat. Ecol. Evol. 4, 270–278 (2020).

    PubMed  Article  PubMed Central  Google Scholar 

  • 25.

    Nicholson, K. E. et al. Mainland colonization by island lizards. J. Biogeogr. 32, 929–938 (2005).

    Article  Google Scholar 

  • 26.

    Poe, S. et al. A phylogenetic, biogeographic, and taxonomic study of all extant species of Anolis (Squamata; Iguanidae). Syst. Biol. 66, 663–697 (2017).

    PubMed  Article  PubMed Central  Google Scholar 

  • 27.

    Jackman, T., Losos, J. B., Larson, A. & de Queiroz, K. in Molecular Evolution and Adaptive Radiation (eds Givnish, T. & Systma, K.) 535–557 (Cambridge University Press, 1997).

  • 28.

    Underwood, G. The anoles of the Eastern Caribbean (Sauria, Iguanidae). Revisionary notes. Bull. Mus. Comp. Zool., Part III 121, 191–226 (1959).

    Google Scholar 

  • 29.

    Losos, J. B. Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles. Vol. 10 (University of California Press, 2009).

  • 30.

    Pinto, G., Mahler, D. L., Harmon, L. J. & Losos, J. B. Testing the island effect in adaptive radiation: rates and patterns of morphological diversification in Caribbean and mainland Anolis lizards. Proc. R. Soc. B 275, 2749–2757 (2008).

    PubMed  Article  PubMed Central  Google Scholar 

  • 31.

    Poe, S. & Anderson, C. G. The existence and evolution of morphotypes in Anolis lizards: coexistence patterns, not adaptive radiations, distinguish mainland and island faunas. PeerJ 6, e6040 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  • 32.

    Irschick, D. J., Vitt, L. J., Zani, P. A. & Losos, J. B. A comparison of evolutionary radiations in mainland and Caribbean Anolis lizards. Ecology 78, 2191–2203 (1997).

    Article  Google Scholar 

  • 33.

    Macrini, T. E., Irschick, D. J. & Losos, J. B. Ecomorphological differences in toepad characteristics between mainland and island anoles. J. Herpetol. 37, 52–58 (2003).

    Article  Google Scholar 

  • 34.

    Velasco, J. A. & Herrel, A. Ecomorphology of Anolis lizards of the Choco’ region in Colombia and comparisons with Greater Antillean ecomorphs. Biol. Biol. J. Linn. Soc. 92, 403–403 (2007).

    Article  Google Scholar 

  • 35.

    Williams, E. E. in Evol. Biol. Vol. 6 (eds Theodosius Dobzhansky, MaxK Hecht, & WilliamC Steere) Ch. 3, 47–89 (Springer US, 1972).

  • 36.

    Williams, E. E. in Lizard ecology: studies of a model organism (eds Pianka, E. R., Huey, R. B. & Schoener, T. W.) 326–370 (Harvard University Press, 1983).

  • 37.

    Losos, J. B., Jackman, T. R., Larson, A., Queiroz, K. & Rodriguez-Schettino, L. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279, 2115–2118 (1998).

    ADS  CAS  PubMed  Article  Google Scholar 

  • 38.

    Tinius, A. & Russell, A. P. Geometric morphometric analysis of the breast-shoulder apparatus of lizards: a test case using Jamaican anoles (Squamata: Dactyloidae). Anat. Rec. 297, 410–432 (2014).

    Article  Google Scholar 

  • 39.

    Tinius, A., Russell, A. P., Jamniczky, H. A. & Anderson, J. S. What is bred in the bone: ecomorphological associations of pelvic girdle form in greater Antillean Anolis lizards. J. Morphol. 279, 1016–1030 (2018).

    PubMed  Article  Google Scholar 

  • 40.

    Adams, D. C. & Collyer, M. L. Phylogenetic comparative methods and the evolution of multivariate phenotypes. Annu. Rev. Ecol. Evol. Syst. 50, 405–425 (2019).

    Article  Google Scholar 

  • 41.

    Legendre, P. & Legendre, L. Numerical Ecology. (Elsevier, 2012).

  • 42.

    Collyer, M. L., Davis, M. A. & Adams, D. C. Making heads or tails of combined landmark configurations in geometric morphometric data. Evol. Biol. 47, 193–205 (2020).

    Article  Google Scholar 

  • 43.

    Kumar, S., Stecher, G., Suleski, M. & Hedges, S. B. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812–1819 (2017).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 44.

    Nishimoto, S. & Logan, M. P. O. Subdivision of the lateral plate mesoderm and specification of the forelimb and hindlimb forming domains. Semin. Cell Dev. Biol. 49, 102–108 (2016).

    PubMed  Article  PubMed Central  Google Scholar 

  • 45.

    Shou, S., Scott, V., Reed, C., Hitzemann, R. & Stadler, H. S. Transcriptome analysis of the murine forelimb and hindlimb autopod. Dev. Dyn. 234, 74–89 (2005).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 46.

    Margulies, E. H., Kardia, S. L. R. & Innis, J. W. A comparative molecular analysis of developing mouse forelimbs and hindlimbs using Serial Analysis of Gene Expression (SAGE). Genome Res. 11, 1686–1698 (2001).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 47.

    Adams, D. C. & Collyer, M. L. On the comparison of the strength of morphological integration across morphometric datasets. Evolution 70, 2623–2631 (2016).

    PubMed  Article  PubMed Central  Google Scholar 

  • 48.

    Adams, D. C. Evaluating modularity in morphometric data: challenges with the RV coefficient and a new test measure. Methods Ecol. Evol. 7, 565–572 (2016).

    Article  Google Scholar 

  • 49.

    Adams, D. C. & Collyer, M. L. Comparing the strength of modular signal, and evaluating alternative modular hypotheses, using covariance ratio effect sizes with morphometric data. Evolution 73, 2352–2367 (2019).

    PubMed  Article  PubMed Central  Google Scholar 

  • 50.

    Dellinger, A. S. et al. Modularity increases rate of floral evolution and adaptive success for functionally specialized pollination systems. Commun. Biol. 2, 453 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  • 51.

    Venditti, C., Meade, A. & Pagel, M. Multiple routes to mammalian diversity. Nature 479, 393–396 (2011).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 52.

    Cooney, C. R. et al. Mega-evolutionary dynamics of the adaptive radiation of birds. Nature 542, 344 (2017).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 53.

    Marki, P. Z., Kennedy, J. D., Cooney, C. R., Rahbek, C. & Fjeldsa, J. Adaptive radiation and the evolution of nectarivory in a large songbird clade. Evolution 73, 1226–1240 (2019).

    PubMed  Article  PubMed Central  Google Scholar 

  • 54.

    Brown, R. L. What evolvability really is. Br. J. Philos. Sci. 65, 549–572 (2013).

    MathSciNet  Article  Google Scholar 

  • 55.

    Watson, R. A. & Szathmary, E. How can evolution learn? Trends Ecol. Evol. 31, 147–157 (2016).

    PubMed  Article  PubMed Central  Google Scholar 

  • 56.

    Young, N. M. & Hallgrimsson, B. Serial homology and the evolution of mammalian limb covariation structure. Evolution 59, 2691–2704 (2005).

    PubMed  Article  PubMed Central  Google Scholar 

  • 57.

    Young, N. M., Wagner, G. P. & Hallgrimsson, B. Development and the evolvability of human limbs. Proc. Natl Acad. Sci. USA 107, 3400–3405 (2010).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 58.

    Kelly, E. M. & Sears, K. E. Reduced phenotypic covariation in marsupial limbs and the implications for mammalian evolution. Biol. J. Linn. Soc. 102, 22–36 (2011).

    Article  Google Scholar 

  • 59.

    Bennett, C. V. & Goswami, A. Does developmental strategy drive limb integration in marsupials and monotremes? Mamm. Biol. 76, 79–83 (2011).

    Article  Google Scholar 

  • 60.

    Martin-Serra, A. & Benson, R. B. J. Developmental constraints do not influence long-term phenotypic evolution of marsupial forelimbs as revealed by interspecific disparity and integration patterns. Am. Nat. 195, 547–560 (2020).

    PubMed  Article  PubMed Central  Google Scholar 

  • 61.

    Parter, M., Kashtan, N. & Alon, U. Facilitated variation: how evolution learns from past environments to generalize to new environments. PLoS Comp. Biol. 4, e1000206 (2008).

    ADS  Article  CAS  Google Scholar 

  • 62.

    Kouvaris, K., Clune, J., Kounios, L., Brede, M. & Watson, R. A. How evolution learns to generalise: Using the principles of learning theory to understand the evolution of developmental organisation. PLoS Comp. Biol. 13, e1005358 (2017).

    ADS  Article  CAS  Google Scholar 

  • 63.

    Brun-Usan, M., Rago, A., Thies, C., Uller, T. & Watson, R. A. Developmental models reveal the role of phenotypic plasticity in explaining genetic evolvability. bioRxiv https://doi.org/10.1101/2020.06.29.179226 (2020).

  • 64.

    Shanahan, T. Phylogenetic inertia and Darwin’s higher law. Stud. Hist. Philos. Sci. Part C 42, 60–68 (2011).

    Article  Google Scholar 

  • 65.

    Houle, D., Bolstad, G. H., van der Linde, K. & Hansen, T. F. Mutation predicts 40 million years of fly wing evolution. Nature 548, 447–450 (2017).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 66.

    Braendle, C., Baer, C. F. & Felix, M. A. Bias and evolution of the mutationally accessible phenotypic space in a developmental system. PLoS Genet. 6, e1000877 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 67.

    Haber, A. Phenotypic covariation and morphological diversification in the ruminant skull. Am. Nat. 187, 576–591 (2016).

    PubMed  Article  PubMed Central  Google Scholar 

  • 68.

    Schluter, D. Adaptive radiation along genetic lines of least resistance. Evolution 50, 1766–1774 (1996).

    PubMed  Article  PubMed Central  Google Scholar 

  • 69.

    Hanot, P., Herrel, A., Guintard, C. & Cornette, R. The impact of artificial selection on morphological integration in the appendicular skeleton of domestic horses. J. Anat. 232, 657–673 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • 70.

    Penna, A., Melo, D., Bernardi, S., Oyarzabal, M. I. & Marroig, G. The evolution of phenotypic integration: How directional selection reshapes covariation in mice. Evolution 71, 2370–2380 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  • 71.

    Watson, R. A., Wagner, G. P., Pavlicev, M., Weinreich, D. M. & Mills, R. The evolution of phenotypic correlations and “developmental memory”. Evolution 68, 1124–1138 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  • 72.

    Donihue, C. M. et al. Hurricane effects on Neotropical lizards span geographic and phylogenetic scales. Proc. Natl Acad. Sci. USA 117, 10429–10434 (2020).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 73.

    Feiner, N., Jackson, I. S. C., Munch, K. L., Radersma, R. & Uller, T. Plasticity and evolutionary convergence in the locomotor skeleton of Greater Antillean Anolis lizards. eLife 9, e57468 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 74.

    Vanhooydonck, B. & Irschick, D. in Topics in functional and ecological vertebrate morphology (eds Aerts, P., D’Août, K., Herrel, A. & Van Damme, R.) (Shaker Publishing, 2002).

  • 75.

    Schluter, D. The Ecology of Adaptive Radiation. (Oxford: Oxford University Press, 2000).

  • 76.

    Roughgarden, J. Anolis Lizards of the Caribbean: Ecology, Evolution, and Plate Tectonics. (Oxford University Press, 1995).

  • 77.

    Stacklies, W., Redestig, H., Scholz, M., Walther, D. & Selbig, J. pcaMethods-a bioconductor package providing PCA methods for incomplete data. Bioinformatics 23, 1164–1167 (2007).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 78.

    Losos, J. B. et al. Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution 54, 301–305 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  • 79.

    Tinius, A. Geometric morphometric analysis of the breast-shoulder apparatus of Greater Antillean anole ecomorphs PhD thesis, (University of Calgary, 2016).

  • 80.

    Cignoni, P. et al. in Eurographics Italian Chapter Conference (eds Scarano, V., De Chiara, R. & Erra, U.) (The Eurographics Association, 2008).

  • 81.

    Geomorph: Software for geometric morphometric analyses. R package version 3.1.0. (2019).

  • 82.

    Olsen, A. M. & Westneat, M. W. StereoMorph: an R package for the collection of 3D landmarks and curves using a stereo camera set-up. Methods Ecol. Evol. 6, 351–356 (2015).

    Article  Google Scholar 

  • 83.

    Mahler, D. L., Ingram, T., Revell, L. J. & Losos, J. B. Exceptional convergence on the macroevolutionary landscape in island lizard radiations. Science 341, 292–295 (2013).

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 84.

    Rohlf, F. J. Shape statistics: procrustes superimpositions and tangent spaces. J. Classif. 16, 197–223 (1999).

    MATH  Article  Google Scholar 

  • 85.

    Uetz, P., Freed, P. & Hosek, J. The Reptile Database http://www.reptile-database.org (2019).

  • 86.

    Pyron, R. A., Burbrink, F. T. & Wiens, J. J. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol. Biol. 13, 93 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 87.

    Köhler, G. & Hedges, S. B. A revision of the green anoles of Hispaniola with description of eight new species (Reptilia, Squamata, Dactyloidae). Nov. Carib. 9, 1–135 (2016).

    Google Scholar 

  • 88.

    Hofmann, E. P. & Townsend, J. H. Origins and biogeography of the Anolis crassulus subgroup (Squamata: Dactyloidae) in the highlands of Nuclear Central America. BMC Evol. Biol. 17, 267 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 89.

    Mahler, D. L. et al. Discovery of a giant chameleon-like lizard (Anolis) on hispaniola and its significance to understanding replicated adaptive radiations. Am. Nat. 188, 357–364 (2016).

    PubMed  Article  PubMed Central  Google Scholar 

  • 90.

    Kohler, J., Hahn, M. & Kohler, G. Divergent evolution of hemipenial morphology in two cryptic species of mainland anoles related to Anolis polylepis. Salamandra 48, 1–11 (2012).

    Google Scholar 

  • 91.

    Kohler, G., Perez, R. G. T., Petersen, C. B. P. & De la Cruz, F. R. M. A revision of the Mexican Anolis (Reptilia, Squamata, Dactyloidae) from the Pacific versant west of the Isthmus de Tehuantepec in the states of Oaxaca, Guerrero, and Puebla, with the description of six new species. Zootaxa 3862, 1 (2014).

    PubMed  Article  PubMed Central  Google Scholar 

  • 92.

    Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).

    Article  Google Scholar 

  • 93.

    Nicholson, K. E., Crother, B. I., Guyer, C. & Savage, J. M. It is time for a new classification of anoles (Squamata: Dactyloidae). Zootaxa 3477, 1–108 (2012).

    Article  Google Scholar 

  • 94.

    Goswami, A. & Finarelli, J. A. EMMLi: a maximum likelihood approach to the analysis of modularity. Evolution 70, 1622–1637 (2016).

    PubMed  Article  PubMed Central  Google Scholar 

  • 95.

    Bookstein, F. L. et al. Cranial integration in Homo: singular warps analysis of the midsagittal plane in ontogeny and evolution. J. Hum. Evol. 44, 167–187 (2003).

    PubMed  Article  PubMed Central  Google Scholar 

  • 96.

    Adams, D. C. Quantifying and comparing phylogenetic evolutionary rates for shape and other high-dimensional phenotypic data. Syst. Biol. 63, 166–177 (2014).

    PubMed  Article  PubMed Central  Google Scholar 

  • 97.

    Xie, W. G., Lewis, P. O., Fan, Y., Kuo, L. & Chen, M. H. Improving marginal likelihood estimation for bayesian phylogenetic model selection. Syst. Biol. 60, 150–160 (2011).

    PubMed  Article  PubMed Central  Google Scholar 

  • 98.

    Brown, M. B. & Forsythe, A. B. Robust tests for the equality of variances. J. Am. Stat. Assoc. 69, 364–367 (1974).

    MATH  Article  Google Scholar 

  • 99.

    Levene, H. in Contributions to Probability and Statistics (Stanford University Press, 1960).

  • 100.

    Kruskal, W. H. & Wallis, W. A. Use of ranks in one-criterion variance analysis. J. Am. Stat. Assoc. 47, 583–621 (1952).

    MATH  Article  Google Scholar 


  • Source: Ecology - nature.com

    Valuing wetlands

    3 Questions: Claude Grunitzky MBA '12 on launching TRUE Africa University