in

Size, microhabitat, and loss of larval feeding drive cranial diversification in frogs

  • 1.

    Collar, D. C., Schulte, J. A., O’Meara, B. C. & Losos, J. B. Habitat use affects morphological diversification in dragon lizards. J. Evol. Biol. 23, 1033–1049 (2010).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 2.

    Da Silva, F. O. et al. The ecological origins of snakes as revealed by skull evolution. Nat. Commun. 9, 1–11 (2018).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 3.

    Vidal-García, M. & Keogh, J. S. Phylogenetic conservatism in skulls and evolutionary lability in limbs – morphological evolution across an ancient frog radiation is shaped by diet, locomotion and burrowing. BMC Evol. Biol. 17, 1–15 (2017).

    Article 

    Google Scholar 

  • 4.

    Fabre, A.-C., Cornette, R., Goswami, A. & Peigné, S. Do constraints associated with the locomotor habitat drive the evolution of forelimb shape? A case study in musteloid carnivorans. J. Anat. 226, 596–610 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 5.

    Dumont, M. et al. Do functional demands associated with locomotor habitat, diet, and activity pattern drive skull shape evolution in musteloid carnivorans? Biol. J. Linn. Soc. 117, 858–878 (2015).

    Article 

    Google Scholar 

  • 6.

    Baeckens, S., Goeyers, C. & Van Damme, R. Convergent evolution of claw shape in a transcontinental lizard radiation. Integr. Comp. Biol. https://doi.org/10.1093/icb/icz151 (2019).

  • 7.

    Price, S. A., Holzman, R., Near, T. J. & Wainwright, P. C. Coral reefs promote the evolution of morphological diversity and ecological novelty in labrid fishes. Ecol. Lett. 14, 462–469 (2011).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 8.

    Price, S. A., Tavera, J. J., Near, T. J. & Wainwright, P. C. Elevated rates of morphological and functional diversification in reef-dwelling haemulid fishes. Evolution 67, 417–428 (2012).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 9.

    Millien, V. Morphological evolution is accelerated among island mammals. PLoS Biol. 4, 1863–1868 (2006).

    CAS 

    Google Scholar 

  • 10.

    Salvidio, S., Crovetto, F. & Adams, D. C. Potential rapid evolution of foot morphology in Italian plethodontid salamanders (Hydromantes strinatii) following the colonization of an artificial cave. J. Evol. Biol. 28, 1403–1409 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 11.

    Ledbetter, N. M. & Bonett, R. M. Terrestriality constrains salamander limb diversification: implications for the evolution of pentadactyly. J. Evol. Biol. 32, 642–652 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 12.

    McGhee Jr, G. R. Convergent Evolution: Limited Forms Most Beautiful (MIT Press, 2011).

  • 13.

    Vullo, R., Allain, R. & Cavin, L. Convergent evolution of jaws between spinosaurid dinosaurs and pike conger eels. Acta Palaeontol. Pol. 61, 825–828 (2016).

    Article 

    Google Scholar 

  • 14.

    Stayton, C. T. Testing hypotheses of convergence with multivariate data: morphological and functional convergence among herbivorous lizards. Evolution 60, 824–841 (2006).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 15.

    Mahler, D. L., Ingram, T., Revell, L. J. & Losos, J. B. Exceptional convergence on the macroevolutionary landscape in island lizard radiations. Science 341, 292–5 (2013).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 16.

    Sears, K. E. Constraints on the morphological evolution of marsupial shoulder girdles. Evolution 58, 2353–2370 (2004).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 17.

    Bennett, C. V. & Goswami, A. Statistical support for the hypothesis of developmental constraint in marsupial skull evolution. BMC Biol. 11, 1–14 (2013).

    Article 

    Google Scholar 

  • 18.

    Goswami, A. et al. Do developmental constraints and high integration limit the evolution of the marsupial oral apparatus? Integr. Comp. Biol. 56, 404–415 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 19.

    Wake, D. B. & Hanken, J. Direct development in the lungless salamanders: what are the consequences for developmental biology, evolution and phylogenesis? Int. J. Dev. Biol. 40, 859–869 (1996).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 20.

    Wake, D. B. & Larson, A. Multidimensional analysis of an evolving lineage. Science 238, 42–48 (1987).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 21.

    Bonett, R. M. & Blair, A. L. Evidence for complex life cycle constraints on salamander body form diversification. Proc. Natl Acad. Sci. USA 114, 9936–9941 (2017).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 22.

    Bardua, C., Wilkinson, M., Gower, D. J., Sherratt, E. & Goswami, A. Morphological evolution and modularity of the caecilian skull. BMC Evol. Biol. 19, 1–23 (2019).

    Article 

    Google Scholar 

  • 23.

    Schlosser, G. in Modularity: Understanding the Development and Evolution of Natural Complex Systems (eds. Callebaut, W. & Rasskin-Gutman, D.) (MIT Press, 2005).

  • 24.

    Moran, N. A. Adaptation and constraint in the complex life cycles of animals. Annu. Rev. Ecol. Syst. 25, 573–600 (1994).

    Article 

    Google Scholar 

  • 25.

    Ebenman, B. Evolution in organisms that change their niches during the life cycle. Am. Nat. 139, 990–1021 (1992).

    Article 

    Google Scholar 

  • 26.

    Mallarino, R. et al. Two developmental modules establish 3D beak-shape variation in Darwin’s finches. Proc. Natl Acad. Sci. USA 108, 4057–4062 (2011).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 27.

    Liedtke, H. C. et al. Terrestrial reproduction as an adaptation to steep terrain in African toads. Proc. R. Soc. B Biol. Sci. 284, 20162598 (2017).

    Article 
    CAS 

    Google Scholar 

  • 28.

    Harrington, S. M., Harrison, L. B. & Sheil, C. A. Ossification sequence heterochrony among amphibians. Evol. Dev. 15, 344–364 (2013).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 29.

    Bonett, R. M., Phillips, J. G., Ledbetter, N. M., Martin, S. D. & Lehman, L. Rapid phenotypic evolution following shifts in life cycle complexity. Proc. R. Soc. B Biol. Sci. 285, 20172304 (2018).

    Article 
    CAS 

    Google Scholar 

  • 30.

    Laurent, R. F. Adaptive modifications in frogs of an isolated highland fauna in Central Africa. Evolution 18, 458–467 (1964).

    Article 

    Google Scholar 

  • 31.

    Moen, D. S., Morlon, H. & Wiens, J. J. Testing convergence versus history: convergence dominates phenotypic evolution for over 150 million years in frogs. Syst. Biol. 65, 146–160 (2016).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 32.

    Moen, D. S., Irschick, D. J. & Wiens, J. J. Evolutionary conservatism and convergence both lead to striking similarity in ecology, morphology and performance across continents in frogs. Proc. R. Soc. B Biol. Sci. 280, 1–9 (2013).

    Google Scholar 

  • 33.

    Duellman, W. E. & Trueb, L. Biology of the Amphibians (McGraw-Hill publishing company, 1986).

  • 34.

    LaBarbera, M. in Patterns and Processes in the History of Life (eds. Raup, D.M. & Jablonski, D.) (Springer, 1986).

  • 35.

    Cardini, A. & Polly, P. D. Larger mammals have longer faces because of size-related constraints on skull form. Nat. Commun. 4, 2458 (2013).

    ADS 
    PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 

  • 36.

    Callery, E. M. & Elinson, R. P. Thyroid hormone-dependent metamorphosis in a direct developing frog. Proc. Natl Acad. Sci. USA 97, 2615–2620 (2000).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 37.

    Ziermann, J. M. & Diogo, R. Cranial muscle development in frogs with different developmental modes: direct development versus biphasic development. J. Morphol. 275, 398–413 (2013).

    Article 

    Google Scholar 

  • 38.

    McDiarmid, R. W. & Altig, R. (eds) Tadpoles: The Biology of Anuran Larvae (University of Chicago Press, 1999).

  • 39.

    Altig, R. & Johnston, G. F. Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetol. Monogr. 3, 81–109 (1989).

    Article 

    Google Scholar 

  • 40.

    Rose, C. S. & Reiss, J. O. in The Skull Volume 1: Development (eds. Hanken, J. & Hall, B. K.) (The University of Chicago Press, 1993).

  • 41.

    Callery, E. M., Fang, H. & Elinson, R. P. Frogs without polliwogs: evolution of anuran direct development. BioEssays 23, 233–241 (2001).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 42.

    Wake, D. B. & Roth, G. (eds). Complex Organismal Functions: Integration and Evolution in Vertebrates (Wiley, Chichester, UK, 1989).

  • 43.

    Weisbecker, V. & Mitgutsch, C. A large-scale survey of heterochrony in anuran cranial ossification patterns. J. Zool. Syst. Evol. Res. 48, 332–347 (2010).

    Article 

    Google Scholar 

  • 44.

    Dehling, J. M. & Sinsch, U. Partitioning of morphospace in larval and adult reed frogs (Anura: Hyperoliidae: Hyperolius) of the Central African Albertine Rift. Zool. Anz. 280, 65–77 (2019).

    Article 

    Google Scholar 

  • 45.

    Phung, T. X., Nascimento, J. C. S., Novarro, A. J. & Wiens, J. J. Correlated and decoupled evolution of adult and larval body size in frogs: larval and adult size evolution. Proc. R. Soc. B Biol. Sci. 287, 20201474 (2020).

    Article 

    Google Scholar 

  • 46.

    Werner, E. E. Amphibian metamorphosis: growth rate, predation risk, and the optimal size at transformation. Am. Nat. 128, 319–341 (1986).

    Article 

    Google Scholar 

  • 47.

    Sherratt, E., Vidal-García, M., Anstis, M. & Keogh, J. S. Adult frogs and tadpoles have different macroevolutionary patterns across the Australian continent. Nat. Ecol. Evol. 1, 1385–1391 (2017).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 48.

    Wollenberg Valero, K. C. et al. Transcriptomic and macroevolutionary evidence for phenotypic uncoupling between frog life history phases. Nat. Commun. 8, 15213 (2017).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 49.

    Trueb, L. in The Skull: Patterns of Structural and Systematic Diversity (eds Hanken, J, & Hall, B. K.) (The University of Chicago Press, 1993).

  • 50.

    Trueb, L. in Evolutionary Biology of the Anurans: Contemporary Research on Major Problems (ed. Vial, J. L.) (University of Missouri Press, 1973).

  • 51.

    Reiss, J. O. The phylogeny of amphibian metamorphosis. Zoology 105, 85–96 (2002).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 52.

    Moore, M. K. & Townsend, V. R. Jr Intraspecific variation in cranial ossification in the tailed frog, Ascaphus truei. J. Herpetol. 37, 714–717 (2003).

    Article 

    Google Scholar 

  • 53.

    Yeh, J. The evolution of development: two portraits of skull ossification in pipoid frogs. Evolution 56, 2484–2498 (2002).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 54.

    Schoch, R. R. Amphibian skull evolution: the developmental and functional context of simplification, bone loss and heterotopy. J. Exp. Zool. B Mol. Dev. Evol. 322B, 619–630 (2014).

    Article 

    Google Scholar 

  • 55.

    Pereyra, M. O. et al. The complex evolutionary history of the tympanic middle ear in frogs and toads (Anura). Sci. Rep. 6, 1–9 (2016).

    Article 
    CAS 

    Google Scholar 

  • 56.

    Long, J. A., Young, G. C., Holland, T., Senden, T. J. & Fitzgerald, E. M. G. An exceptional Devonian fish from Australia sheds light on tetrapod origins. Nature 444, 199–202 (2006).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 57.

    Daeschler, E. B., Shubin, N. H. & Jenkins, F. A. Jr A Devonian tetrapod-like fish and the evolution of the tetrapod body plan. Nature 440, 757–763 (2006).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 58.

    Barton, R. A. & Harvey, P. H. Mosaic evolution of brain structure in mammals. Nature 405, 1055–1058 (2000).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 59.

    Schlosser, G. Mosaic evolution of neural development in anurans: acceleration of spinal cord development in the direct developing frog Eleutherodactylus coqui. Anat. Embryol. 206, 215–227 (2003).

    Article 

    Google Scholar 

  • 60.

    Felice, R. N. & Goswami, A. Developmental origins of mosaic evolution in the avian cranium. Proc. Natl Acad. Sci. USA 115, 555–560 (2018).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 61.

    Felice, R. N. et al. Evolutionary integration and modularity in the archosaur cranium. Integr. Comp. Biol. 59, 371–382 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 62.

    Watanabe, A. et al. Ecomorphological diversification in squamates from conserved pattern of cranial integration. Proc. Natl Acad. Sci. USA 116, 14688–14697 (2019).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 63.

    Owen, R. On the Archaeopteryx of Von Meyer, with a description of the fossil remains of a long-tailed species from the lithographic stone of Solnhofen. Philos. Trans. R. Soc. Lond. 153, 33–47 (1863).

    ADS 

    Google Scholar 

  • 64.

    Paluh, D. J., Stanley, E. L. & Blackburn, D. C. Evolution of hyperossification expands skull diversity in frogs. Proc. Natl Acad. Sci. USA 117, 8554–8562 (2020).

  • 65.

    Gomez-Mestre, I., Pyron, R. A. & Wiens, J. J. Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs. Evolution 66, 3687–3700 (2012).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 66.

    Nevo, E. Adaptive convergence and divergence of subterranean mammals. Annu. Rev. Ecol. Syst. 10, 269–308 (1979).

    Article 

    Google Scholar 

  • 67.

    Nevo, E. Mammalian evolution underground. The ecological-genetic-phenetic interfaces. Acta Theriol. 3, 9–31 (1995).

    Article 

    Google Scholar 

  • 68.

    Vogel, S. Life’s Devices: The Physical World of Animals and Plants (Princeton Univ. Press, 1988).

  • 69.

    Sansalone, G. et al. Impact of transition to a subterranean lifestyle on morphological disparity and integration in talpid moles (Mammalia, Talpidae). BMC Evol. Biol. 19, 1–15 (2019).

    CAS 
    Article 

    Google Scholar 

  • 70.

    Nauwelaerts, S., Ramsay, J. & Aerts, P. Morphological correlates of aquatic and terrestrial locomotion in a semi-aquatic frog, Rana esculenta: no evidence for a design conflict. J. Anat. 210, 304–317 (2007).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 71.

    Sherratt, E., Gower, D. J., Klingenberg, C. P. & Wilkinson, M. Evolution of cranial shape in caecilians (Amphibia: Gymnophiona). Evol. Biol. 41, 528–545 (2014).

    Article 

    Google Scholar 

  • 72.

    Cardini, A., Polly, P. D., Dawson, R. & Milne, N. Why the long face? Kangaroos and wallabies follow the same ‘rule’ of cranial evolutionary allometry (CREA) as placentals. Evol. Biol. 42, 169–176 (2015).

    Article 

    Google Scholar 

  • 73.

    Yeh, J. The effect of miniaturized body size on skeletal morphology in frogs. Evolution 56, 628–641 (2002).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 74.

    Wells, K. D. The Ecology and Behavior of Amphibians (University of Chicago Press, 2010).

  • 75.

    Emerson, S. B. Skull shape in frogs: correlations with diet. Herpetologica 41, 177–188 (1985).

    Google Scholar 

  • 76.

    Carreño, C. A. & Nishikawa, K. C. Aquatic feeding in pipid frogs: the use of suction for prey capture. J. Exp. Biol. 213, 2001–2008 (2010).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 77.

    Fernandez, E., Irish, F. & Cundall, D. How a frog, Pipa pipa, succeeds or fails in catching fish. Copeia 105, 108–119 (2017).

    Article 

    Google Scholar 

  • 78.

    Herrel, A. et al. in Feeding in Vertebrates: Evolution, Morphology, Behavior, Biomechanics (eds. Bels, V. & Whishaw, I. Q.) (Springer, 2019).

  • 79.

    Bardua, C. et al. Evolutionary integration of the frog cranium. Evolution 74, 1200–1215 (2020).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 80.

    Bon, M., Bardua, C., Goswami, A. & Fabre, A.-C. Cranial integration in the fire salamander, Salamandra salamandra (Caudata: Salamandridae). Biol. J. Linn. Soc. 130, 178–194 (2020).

  • 81.

    Fabre, A. et al. Metamorphosis and the evolution of morphological diversity in salamanders. Nat. Ecol. Evol. 4, 1129–1140 (2020).

  • 82.

    Nishikawa, K. C. in Feeding: Form, Function and Evolution in Tetrapod Vertebrates (ed. Schwenk, K.) (Academic Press, 2000).

  • 83.

    Trueb, L. & Gans, C. Feeding specializations of the Mexican burrowing toad, Rhinophrynus dorsalis (Anura: Rhinophrynidae). J. Zool. 199, 189–208 (1983).

    Article 

    Google Scholar 

  • 84.

    Nishikawa, K. C., Kier, W. M. & Smith, K. K. Morphology and mechanics of tongue movement in the African pig-nosed frog Hemisus marmoratum: a muscular hydrostatic model. J. Exp. Biol. 202, 771–80 (1999).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 85.

    Henrici, A. C. Digging through the past: the evolutionary history of burrowing and underground feeding in rhinophrynid anurans. Palaeobiodivers. Palaeoenviron. 96, 97–109 (2015).

    Article 

    Google Scholar 

  • 86.

    Van Dijk, D. E. Osteology of the ranoid burrowing African anurans Breviceps and Hemisus. Afr. Zool. 36, 137–141 (2001).

    Article 

    Google Scholar 

  • 87.

    Womack, M. C., Christensen-Dalsgaard, J., Coloma, L. A. & Hoke, K. L. Sensitive high-frequency hearing in earless and partially eared harlequin frogs (Atelopus). J. Exp. Biol. 221, 1–8 (2018).

    Article 

    Google Scholar 

  • 88.

    Boistel, R. et al. How minute sooglossid frogs hear without a middle ear. Proc. Natl Acad. Sci. USA 110, 15360–15364 (2013).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 89.

    Womack, M. C., Stynoski, J. L., Voyles, M. K., Coloma, L. A. & Hoke, K. L. Prolonged middle ear development in Rhinella horribilis. J. Morphol. 279, 1518–1523 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 90.

    Womack, M. C., Christensen-Dalsgaard, J., Coloma, L. A., Chaparro, J. C. & Hoke, K. L. Earless toads sense low frequencies but miss the high notes. Proc. R. Soc. B Biol. Sci. 284, 20171670 (2017).

    Article 

    Google Scholar 

  • 91.

    Hetherington, T. E. in The Evolutionary Biology of Hearing (eds. Webster, D. B., Fay, R. R. & Popper, A. N.) (Springer, 1992).

  • 92.

    Hanken, J., Klymkowsky, M. W., Summers, C. H., Seufert, D. W. & Ingebrigtsen, N. Cranial ontogeny in the direct-developing frog, Eleutherodactylus coqui (Anura: Leptodactylidae), analyzed using whole-mount lmmunohistochemistry. J. Morphol. 211, 95–118 (1992).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 93.

    Hanken, J., Klymkowsky, M. W., Alley, K. E. & Jennings, D. H. Jaw muscle development as evidence for embryonic repatterning in direct-developing frogs. Proc. R. Soc. B Biol. Sci. 264, 1349–1354 (1997).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • 94.

    Wray, G. A. & Raff, R. A. The evolution of developmental strategy in marine invertebrates. Trends Ecol. Evol. 6, 45–50 (1991).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 95.

    Watkins, T. B. A quantitative genetic test of adaptive decoupling across metamorphosis for locomotor and life-history traits in the Pacific tree frog, Hyla regilla. Evolution 55, 1668–1677 (2001).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 96.

    Wilson, A. D. M. & Krause, J. Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav. Ecol. 23, 1316–1323 (2012).

    Article 

    Google Scholar 

  • 97.

    O’Reilly, J. C., Deban, S. M. & Nishikawa., K. C. in Topics in Functional and Ecological Vertebrate Morphology: A Tribute to Frits de Vree (eds. Aerts, P., D’Août, K., Herrel, A. & van Damme, R.) (Shaker Publishing, 2002).

  • 98.

    Philips, P. C. Genetic constraints at the metamorphic boundary: morphological development in the wood frog, Rana sylvatica. J. Evol. Biol. 11, 453–463 (1998).

    Article 

    Google Scholar 

  • 99.

    Johansson, F., Lederer, B. & Lind, M. I. Trait performance correlations across life stages under environmental stress conditions in the common frog, Rana temporaria. PLoS ONE 5, e11680 (2010).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 100.

    Wassersug, R. J. The adaptive significance of the tadpole stage with comments on the maintenance of complex life cycles in anurans. Am. Zool. 15, 405–417 (1975).

    Article 

    Google Scholar 

  • 101.

    Vassilieva, A. B. Heterochronies in the cranial development of Asian tree frogs (Amphibia: Anura: Rhacophoridae) with different life histories. Dokl. Biol. Sci. 473, 110–113 (2017).

    Article 

    Google Scholar 

  • 102.

    Kerney, R., Meegaskumbura, M., Manamendra-Arachchi, K. & Hanken, J. Cranial ontogeny in Philautus silus (Anura: Ranidae: Rhacophorinae) reveals few similarities with other direct-developing anurans. J. Morphol. 268, 715–725 (2007).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 103.

    Heatwole, H. & Davies, M. (eds.) Amphibian biology (volume 5), osteology. (Surrey Beatty & Sons, 2003).

  • 104.

    Hanken, J. & Hall, B. K. Skull development during anuran metamorphosis: I. Early development of the first three bones to form–the exoccipital, the parasphenoid, and the frontoparietal. J. Morphol. 195, 247–256 (1988).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 105.

    Fink, W. L. The conceptual relationship between ontogeny and phylogeny. Paleobiology 8, 254–264 (1982).

    Article 

    Google Scholar 

  • 106.

    Strathmann, R. R. in Echinoderm Phylogeny and Evolutionary Biology (eds. Paul, C. R. C. & Smith, A. B.) (Clarendon Press, 1988).

  • 107.

    Laloy, F. et al. A re-interpretation of the Eocene anuran Thaumastosaurus based on MicroCT examination of a “mummified” specimen. PLoS ONE 8, e74874 (2013).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 108.

    Frost, D. R. et al. The amphibian tree of life. Bull. Am. Mus. Nat. Hist. 297, 1–370 (2006).

  • 109.

    Quental, T. B. & Marshall, C. R. Diversity dynamics: molecular phylogenies need the fossil record. Trends Ecol. Evol. 25, 435–441 (2010).

    Article 

    Google Scholar 

  • 110.

    Slater, G. J. & Harmon, L. J. Unifying fossils and phylogenies for comparative analyses of diversification and trait evolution. Methods Ecol. Evol. 4, 699–702 (2013).

    Article 

    Google Scholar 

  • 111.

    Volume Graphics. VGStudio MAX v. 2.0 (Volume Graphics GmbH, 2001).

  • 112.

    Bardua, C., Felice, R. N., Watanabe, A., Fabre, A.-C. & Goswami, A. A practical guide to sliding and surface semilandmarks in morphometric analyses. Integr. Org. Biol. 1, 1–34 (2019).

    Google Scholar 

  • 113.

    Jetz, W. & Pyron, R. A. The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat. Ecol. Evol. 2, 850–858 (2018).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 114.

    Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).

    CAS 
    Article 

    Google Scholar 

  • 115.

    Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 35, 526–528 (2018).

    Article 
    CAS 

    Google Scholar 

  • 116.

    Wiley, D. F. et al. Evolutionary morphing. In Proc. Visualization Conference (IEEE, 2005).

  • 117.

    Schlager, S. in Statistical Shape and Deformation Analysis (eds. Zheng, G., Li, S. & Szekely, G.) (Academic Press, 2017).

  • 118.

    Cardini, A. Left, right or both? Estimating and improving accuracy of one-side-only geometric morphometric analyses of cranial variation. J. Zool. Syst. Evol. Res. 55, 1–10 (2016).

    Article 

    Google Scholar 

  • 119.

    Marshall, A. F. et al. High-density three-dimensional morphometric analyses support conserved static (intraspecific) modularity in caecilian (Amphibia: Gymnophiona) crania. Biol. J. Linn. Soc. 126, 721–742 (2019).

    Article 

    Google Scholar 

  • 120.

    Bossuyt, F. & Milinkovitch, M. C. Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proc. Natl Acad. Sci. USA 97, 6585–90 (2000).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 121.

    Young, J. E., Christian, K. A., Donnellan, S. C., Tracy, C. R. & Parry, D. Comparative analysis of cutaneous evaporative water loss in frogs demonstrates correlation with ecological habits. Physiol. Biochem. Zool. 78, 847–856 (2005).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 122.

    Portik, D. M. & Blackburn, D. C. The evolution of reproductive diversity in Afrobatrachia: a phylogenetic comparative analysis of an extensive radiation of African frogs. Evolution 70, 2017–2032 (2016).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 123.

    Scott, E. A phylogeny of ranid frogs (Anura: Ranoidea: Ranidae), based on a simultaneous analysis of morphological and molecular data. Cladistics 21, 507–574 (2005).

    Article 

    Google Scholar 

  • 124.

    Adams, D. C. & Otárola-Castillo, E. geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4, 393–399 (2013).

    Article 

    Google Scholar 

  • 125.

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

    Article 

    Google Scholar 

  • 126.

    Clavel, J., Escarguel, G. & Merceron, G. mvmorph: an r package for fitting multivariate evolutionary models to morphometric data. Methods Ecol. Evol. 6, 1311–1319 (2015).

    Article 

    Google Scholar 

  • 127.

    Clavel, J., Aristide, L. & Morlon, H. A penalized likelihood framework for high-dimensional phylogenetic comparative methods and an application to new-world monkeys brain evolution. Syst. Biol. 68, 93–116 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 128.

    Clavel, J. & Morlon, H. Reliable phylogenetic regressions for multivariate comparative data: illustration with the MANOVA and application to the effect of diet on mandible morphology in phyllostomid bats. Syst. Biol. 69, 927–943 (2020).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 129.

    Housworth, E. A., Martins, E. P. & Lynch, M. The phylogenetic mixed model. Am. Nat. 163, 84–96 (2004).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 130.

    Revell, L. J. Phylogenetic signal and linear regression on species data. Methods Ecol. Evol. 1, 319–329 (2010).

    Article 

    Google Scholar 

  • 131.

    Freckleton, R. P., Harvey, P. H. & Pagel, M. Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712–726 (2002).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 132.

    Goolsby, E. W., Bruggeman, J. & Ane, C. Rphylopars: phylogenetic comparative tools for missing data and within-species variation. R package version 0.2.11 https://CRAN.R-project.org/package=Rphylopars (2019).

  • 133.

    Goolsby, E. W., Bruggeman, J. & Ané, C. Rphylopars: fast multivariate phylogenetic comparative methods for missing data and within-species variation. Methods Ecol. Evol. 8, 22–27 (2017).

    Article 

    Google Scholar 

  • 134.

    Bardua, C. & Goswami, A. Frog skull shape data for modularity and macroevolution. https://doi.org/10.5281/zenodo.4619880 (2020).


  • Source: Ecology - nature.com

    Invitations to powerful climate action at MIT Better World (Sustainability)

    Climate solutions depend on technology, policy, and businesses working together