Physiological constraints on body size distributions in Crocodyliformes.


Journal

Evolution; international journal of organic evolution
ISSN: 1558-5646
Titre abrégé: Evolution
Pays: United States
ID NLM: 0373224

Informations de publication

Date de publication:
02 2020
Historique:
received: 05 04 2019
revised: 21 11 2019
accepted: 30 11 2019
pubmed: 17 1 2020
medline: 3 10 2020
entrez: 17 1 2020
Statut: ppublish

Résumé

At least 26 species of crocodylian populate the globe today, but this richness represents a minute fraction of the diversity and disparity of Crocodyliformes. Fossil forms are far more varied, spanning from erect, fully terrestrial species to flippered, fully marine species. To quantify the influence of a marine habitat on the directionality, rate, and variance of evolution of body size in Crocodyliformes and thereby identify underlying selective pressures, we compiled a database of body sizes for 264 fossil and modern species of crocodyliform covering terrestrial, semi-aquatic, and marine habitats. We find increases in body size coupled with increases in strength of selection and decreases in variance following invasions of marine habitats but not of semiaquatic habitats. A model combining constraints from thermoregulation and lung capacity provides a physiological explanation for the larger minimum and average sizes of marine species. It appears that constraints on maximum size are shared across Crocodyliformes, perhaps through factors such as the allometric scaling of feeding rate versus basal metabolism with body size. These findings suggest that broad-scale patterns of body size evolution and the shapes of body size distributions within higher taxa are often determined more by physiological constraints than by ecological interactions or environmental fluctuations.

Identifiants

pubmed: 31943148
doi: 10.1111/evo.13901
doi:

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

245-255

Subventions

Organisme : U.S. National Science Foundation
ID : EAR-1151022 to JLP
Pays : International
Organisme : Division of Earth Sciences
ID : 1151022
Pays : International

Informations de copyright

© 2020 The Authors. Evolution © 2020 The Society for the Study of Evolution.

Références

Anderson, J. F., R. Hermann, and H. D. Prange. 1979. Scaling of supportive tissue mass. Q. Rev. Biol. 54:139-148.
Bapst, D. W. 2012. paleotree: an R package for paleontological and phylogenetic analyses of evolution. Methods Ecol. Evol. 3:803-807.
Beaulieu, J. M., D.-C. Jhwueng, C. Boettiger, and B. C. O'Meara. 2012. Modeling stabilizing selection: expanding the Ornstein-Uhlenbeck model of adaptive evolution. Evolution 66:2369-2383.
Benson, R. B. J., R. A. Frigot, A. Goswami, B. Andres, and R. J. Butler. 2014. Competition and constraint drove Cope's rule in the evolution of giant flying reptiles. Nat. Commun. 5:3567.
Berta, A., J. L. Sumich, K. M. Kovacs, P. A. Folkens, and P. J. Adam. 2006. Respiration and diving physiology. Pp. 237-269 in Marine mammals. Elsevier, Amsterdam, The Netherlands.
Brochu, C. A. 2013. Phylogenetic relationships of Palaeogene ziphodont eusuchians and the status of Pristichampsus Gervais, 1853. Earth Environ. Sci. Trans. R. Soc. Edinburgh 103:521-550.
Bronzati, M., F. C. Montefeltro, and M. C. Langer. 2012. A species-level supertree of Crocodyliformes. Hist. Biol. 24:598-606.
Bronzati, M., F. C. Montefeltro, and M. C. Langer 2015. Diversification events and the effects of mass extinctions on Crocodyliformes evolutionary history. R. Soc. Open Sci 2:140385.
Brusatte, S. L., M. J. Benton, M. Ruta, and G. T. Lloyd. 2008. Superiority, competition, and opportunism in the evolutionary radiation of dinosaurs. Science 321:1485-1488.
Buckley, G. A., C. A. Brochu, D. W. Krause, and D. Pol. 2000. A pug-nosed crocodyliform from the late cretaceous of Madagascar. Nature 405:941-944.
Burness, G. P., J. Diamond, and T. Flannery. 2001. Dinosaurs, dragons, and dwarfs: the evolution of maximal body size. Proc. Natl. Acad. Sci. USA 98:14518-14523.
Burnham, K. P., and D. R. Anderson. 2002. Model selection and multimodel inference. Springer, New York, NY.
Butler, M., and A. King. 2004. Phylogenetic comparative analysis: a modeling approach for adaptive evolution. Am. Nat. 164:683-695.
Clauset, A., and D. H. Erwin. 2008. The evolution and distribution of species body size. Science 321:399-401.
Cott, H. B. 1961. Scientific results of an inquiry into the ecology and economic status of the Nile Crocodile (Crocodilus niloticus) in Uganda and Northern Rhodesia. Trans. Zool. Soc. London 29:211-356.
Cramer, D. 1998. Fundamental statistics for social research. Routledge, New York.
Downhower, J. F., and L. S. Bulmer. 1988. Calculating just how small a whale can be. Nature 335:675.
Ernest, S. K. M., J. H. Brown, T. Dayan, B. Tiffney, M. R. Willig, J. Alroy, J. P. Haskell, W. P. Porter, P. A. Marquet, K. E. Jones, et al. 2004. Similarity of mammalian body size across the taxonomic hierarchy and across space and time. Am. Nat. 163:672-691.
Farlow, J. O., G. R. Hurlburt, R. M. Elsey, A. R. C. Britton, and W. Langston. 2005. Femoral dimensions and body size of Alligator mississippiensis: estimating the size of extinct mesoeucrocodylians. J. Vertebr. Paleontol. 25:354-369.
Gearty, W., C. R. McClain, and J. L. Payne. 2018. Energetic tradeoffs control the size distribution of aquatic mammals. Proc. Natl. Acad. Sci. USA 115:4194-4199.
Godoy, P. L., R. B. J. Benson, M. Bronzati, and R. J. Butler. 2019. The multi-peak adaptive landscape of crocodylomorph body size evolution. BMC Evol. Biol. 19:167.
Gomani, E. M. 1997. A crocodyliform from the early cretaceous dinosaur beds, northern Malawi. J. Vertebr. Paleontol. 17:280-294.
Hansen, T. F. 1997. Stabilizing selection and the comparative analysis of adaptation. Evolution 51:1341.
Hansen, T. F., J. Pienaar, and S. H. Orzack. 2008. A comparative method for studying adaptation to a randomly evolving environment. Evolution 62:1965-1977.
Heim, N. A., J. L. Payne, S. Finnegan, M. L. Knope, M. Kowalewski, S. K. Lyons, D. W. McShea, P. M. Novack-Gottshall, F. A. Smith, and S. C. Wang. 2017. Hierarchical complexity and the size limits of life. Proc. R. Soc. B Biol. Sci. 284:20171039.
Holland, H. D. 2006. The oxygenation of the atmosphere and oceans. Philos. Trans. R. Soc. B Biol. Sci. 361:903-915.
Hua, S., and V. De Buffrenil. 1996. Bone histology as a clue in the interpretation of functional adaptations in the Thalattosuchia (Reptilia, Crocodylia). J. Vertebr. Paleontol. 16:703-717.
Huelsenbeck, J. P., R. Nielsen, J. P. Bollback, and T. Schultz. 2003. Stochastic mapping of morphological characters. Syst. Biol. 52:131-158.
Jaffe, A. L., G. J. Slater, and M. E. Alfaro. 2011. The evolution of island gigantism and body size variation in tortoises and turtles. Biol. Lett. 7:558-561.
Jouve, S., B. Mennecart, J. Douteau, and N. Jalil. 2017. Biases in the study of relationships between biodiversity dynamics and fluctuation of environmental conditions. Palaeontol. Electron. https://doi.org/10.26879/723.
Mannion, P. D., R. B. J. Benson, M. T. Carrano, J. P. Tennant, J. Judd, and R. J. Butler. 2015. Climate constrains the evolutionary history and biodiversity of crocodylians. Nat. Commun. 6:8438.
Matzke, N. J., and A. Wright. 2016. Inferring node dates from tip dates in fossil Canidae: the importance of tree priors. Biol. Lett. 12:20160328.
Maurer, B. A., J. H. Brown, and R. D. Rusler. 1992. The micro and macro in body size evolution. Evolution 46:939-953.
O'Connor, P. M., J. J. W. Sertich, N. J. Stevens, E. M. Roberts, M. D. Gottfried, T. L. Hieronymus, Z. A. Jinnah, R. Ridgely, S. E. Ngasala, and J. Temba. 2010. The evolution of mammal-like crocodyliforms in the cretaceous period of Gondwana. Nature 466:748-751.
O'Meara, B. C., C. Ané, M. J. Sanderson, and P. C. Wainwright. 2006. Testing for different rates of continuous trait evolution using likelihood. Evolution 60:922.
Pawar, S., A. I. Dell, and V. M. Savage. 2012. Dimensionality of consumer search space drives trophic interaction strengths. Nature 486:485-489.
Pol, D., and M. a. Norell. 2004. A new gobiosuchid crocodyliform taxon from the Cretaceous of Mongolia. Am. Museum Novit. 3458:1-31.
Prange, H. D., J. F. Anderson, and H. Rahn. 1979. Scaling of skeletal mass to body mass in birds and mammals. Am. Nat. 113:103-122.
Price, S. A., and S. S. B. Hopkins. 2015. The macroevolutionary relationship between diet and body mass across mammals. Biol. J. Linn. Soc. 115:173-184.
Rambaut, A., A. J. Drummond, D. Xie, G. Baele, and M. A. Suchard. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67:901-904.
Revell, L. J. 2012. Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3:217-223.
Reynolds, W. W., and W. J. Karlotski. 1977. The allometric relationship of skeleton weight to body weight in teleost fishes: a preliminary comparison with birds and mammals. Copeia 1977:160.
Ronquist, F., M. Teslenko, P. van der Mark, D. L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M. A. Suchard, and J. P. Huelsenbeck. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542.
Schmidt-Nielsen, K. 1971. Locomotion: energy cost of swimming, flying, and running. Science 177:222-228.
Schmidt-Nielsen, K. 1984. Scaling: why is animal size so important? Cambridge Univ. Press, Cambridge, U.K.
Sereno, P. C., H. C. E. Larsson, C. A. Sidor, and B. Gado. 2001. The giant crocodyliform Sarcosuchus from the cretaceous of Africa. Science 294:1516-1519.
Seymour, R. S. 1982. Physiological adaptations to aquatic life. Pp. 1-50 in C. Gans and F. H. Pough, eds. Biology of the Reptilia, Vol. 13 physiology D. Academic Press, London.
Seymour, R. S., C. L. Bennett-Stamper, S. D. Johnston, D. R. Carrier, and G. C. Grigg. 2004. Evidence for endothermic ancestors of crocodiles at the stem of archosaur evolution. Physiol. Biochem. Zool. 77:1051-1067.
Seymour, R. S., C. M. Gienger, M. L. Brien, C. R. Tracy, S. Charlie Manolis, G. J. W. Webb, and K. A. Christian. 2013. Scaling of standard metabolic rate in estuarine crocodiles Crocodylus porosus. J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 183:491-500.
Shurin, J. B., D. S. Gruner, and H. Hillebrand. 2006. All wet or dried up? Real differences between aquatic and terrestrial food webs. Proc. R. Soc. B Biol. Sci. 273:1-9.
Smith, E. N. 1979. Behavioral and physiological thermoregulation of crocodilians. Integr. Comp. Biol. 19:239-247.
Smith, E. N. 1976. Heating and cooling rates of the American alligator, Alligator mississippiensis. Physiol. Zool. 49:37-48.
Steel, R. 1973. Crocodylia. Handbuch der Paläoherpetologie, Teil 16. Gustav Fischer Verlag, Stuttgart.
Sugiura, N. 1978. Further analysis of the data by Akaike's information criterion and the finite corrections. Commun. Stat. 7:13-26.
Tennant, J. P., P. D. Mannion, and P. Upchurch. 2016. Environmental drivers of crocodyliform diversity and extinction through the Jurassic/cretaceous boundary. Proc. R. Soc. B 283:140.
Tucker, M. A., and T. L. Rogers. 2014. Examining predator-prey body size, trophic level and body mass across marine and terrestrial mammals. Proc. R. Soc. B Biol. Sci. 281:1-9.
Tucker, M. A., T. J. Ord, and T. L. Rogers. 2014. Evolutionary predictors of mammalian home range size: body mass, diet and the environment. Glob. Ecol. Biogeogr. 23:1105-1114.
Vermeij, G. J. 1994. The evolutionary interaction among species: selection, escalation, and coevolution. Annu. Rev. Ecol. Syst. 25:219-236.
Wilberg, E. W., A. H. Turner, and C. A. Brochu. 2019. Evolutionary structure and timing of major habitat shifts in Crocodylomorpha. Sci. Rep. 9:514.
Williams, T. M. 1999. The evolution of cost efficient swimming in marine mammals: limits to energetic optimization. Philos. Trans. R. Soc. B Biol. Sci. 354:193-201.
Wright, J. C., and D. S. Kirshner. 1987. Allometry of lung volume during voluntary submergence in the saltwater crocodile crocodylus porosus. J. Exp. Biol. 130:433-436.
Young, M., M. Rabi, M. Bell, D. Foffa, L. Steel, S. Sachs, and K. Peyer. 2016. Big-headed marine crocodyliforms and why we must be cautious when using extant species as body length proxies for long-extinct relatives. Palaeontol. Electron. https://doi.org/10.26879/648.
Young, M. T., S. L. Brusatte, M. Ruta, and M. B. De Andrade. 2010. The evolution of Metriorhynchoidea (mesoeucrocodylia, thalattosuchia): an integrated approach using geometric morphometrics, analysis of disparity, and biomechanics. Zool. J. Linn. Soc. 158:801-859.
Young, M. T., M. A. Bell, M. B. de Andrade, and S. L. Brusatte. 2011. Body size estimation and evolution in metriorhynchid crocodylomorphs: implications for species diversification and niche partitioning. Zool. J. Linn. Soc. 163:1199-1216.
Young, M. T., S. L. Brusatte, M. B. de Andrade, J. B. Desojo, B. L. Beatty, L. Steel, M. S. Fernández, M. Sakamoto, J. I. Ruiz-Omeñaca, and R. R. Schoch. 2012. The cranial osteology and feeding ecology of the metriorhynchid crocodylomorph genera Dakosaurus and Plesiosuchus from the late Jurassic of Europe. PLoS One 7:e44985.
Zanno, L. E., S. Drymala, S. J. Nesbitt, and V. P. Schneider. 2015. Early crocodylomorph increases top tier predator diversity during rise of dinosaurs. Sci. Rep. 5:9276.

Auteurs

William Gearty (W)

School of Biological Sciences, University of Nebraska-Lincoln, Lincoln, Nebraska, 68588.
Department of Geological Sciences, Stanford University, Stanford, California, 94305.

Jonathan L Payne (JL)

Department of Geological Sciences, Stanford University, Stanford, California, 94305.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH