Body Size Evolution in Crocodylians and Their Extinct Relatives

Abstract

Crocodylians are currently facing evolutionary decline. This is evinced by the rich fossil record of their extinct relatives, crocodylomorphs, which show not only significantly higher levels of biodiversity in the past but also remarkable morphological disparity and higher ecological diversity. In terms of body size, crocodylians are mostly large animals (>2 m), especially when compared to other extant reptiles. In contrast, extinct crocodylomorphs exhibited a 10‐fold range in body sizes, with early terrestrial forms often quite small. Recent research has shed new light on the tempo and mode of crocodylomorph body size evolution, demonstrating a close relationship with ecology, in which physiological constraints contribute to the larger sizes of marine species. Abiotic environmental factors can also play an important role within individual subgroups. Crocodylians, for instance, have been experiencing an average size increase during Cenozoic, which seems to be related to a long‐term process of global cooling.

Key Concepts

  • Although Crocodylia is currently a depauperate group, the fossil record of its closest extinct relatives, crocodylomorphs, can provide important evidence to answer major evolutionary questions, such as on extinction and diversity loss.
  • Crocodylomorph body size has varied significantly over time, as well as between subgroups, ranging from relatively small (<1 m) to gigantic (>10 m) species.
  • Crocodylomorph body size evolution is not consistent with an overall trend towards large or smaller sizes through time; instead, multiple shifts to different evolutionary regimes can explain the observed body size values.
  • Climate alone cannot explain the evolution of body size in all crocodylomorphs, but some environmental factors had stronger influence on individual subgroups.
  • The usually larger sizes of aquatic and marine crocodylomorphs can be explained by physiological constraints associated with thermoregulation and lung capacity when under the water.
  • A strong correlation between temperature and body size found for members of the crown‐group (Crocodylia) indicates that species became larger on average as the world became cooler during the Cenozoic.

Keywords: body size; Crocodylomorpha; Crocodylia; macroevolution; phylogenetic comparative methods; adaptive landscape

Figure 1. On the left, examples of extant crocodylians, which show similar overall body plan and ecology: (a) Crocodylus porosus. (b) Alligator mississippiensis. (c) Gavialis gangeticus. On the right, skulls of some extinct crocodylomorph in dorsal view, illustrating the morphological and size variation exhibited by the group: (d) Dibothrosuchus elpahros. (e) Simosuchus clarki. (f) Montealtosuchus arrudacamposi. (g) Steneosaurus bollensis. (h) Sarcosuchus imperator. (i) Ikanogavialis gameroi. All skulls of extinct crocodylomorphs are to the same scale (scale bar = 15 cm). Source: Photographs of living crocodylians taken by Ilham Nurwansah, J. Philipp Krone, and Ryan Somma
Figure 2. Phylogenetic relationships among most important crocodylomorph subgroups (shown in different colours). Silhouettes of some representatives of these groups are included in coloured boxes and are size‐scaled to illustrate the diversity of body sizes in the group. Sources: Bronzati M, Montefeltro FC and Langer MC () Diversification events and the effects of mass extinctions on Crocodyliformes evolutionary history. Royal Society Open Science 2: 140385; Godoy PL, Benson RB, Bronzati M and Butler RJ () The multi‐peak adaptive landscape of crocodylomorph body size evolution. BMC Evolutionary Biology 19: 167; Wilberg EW, Turner AH and Brochu CA () Evolutionary structure and timing of majorhabitat shifts in Crocodylomorpha. Scientific Reports 9: 514.
Figure 3. Patterns of crocodylomorph body size through time and between subgroups. Body size is represented by a cranial measurement (dorsal orbito‐cranial length) after log‐transformation. (a) Mean body size (red line) through time, with lower and upper limits (i.e. minimum and maximum size) of each time bin represented by light red shaded area. (b) Body size disparity (sum of variances) through time. Error bars represent bootstrapped values (500 replicates). (c) Phenogram with body size incorporated into crocodylomorph phylogeny, with most important crocodylomorph subgroups shown in different colours. (d) Mean body size of different subgroups (mean values were subjected to bootstraps and rarefaction; colour key same as panel c). (e) Body size disparity (sum of variances) of different subgroups (disparity values were subjected to bootstraps and rarefaction; colour key same as panel c). Data from Godoy PL, Benson RB, Bronzati M and Butler RJ () The multi‐peak adaptive landscape of crocodylomorph body size evolution. BMC Evolutionary Biology 19: 167.
Figure 4. Body size patterns of different crocodylomorph lifestyles (terrestrial, semi‐aquatic/freshwater and aquatic/marine). Body size is represented by a cranial measurement (dorsal orbito‐cranial length) after log‐transformation. (a) Mean body size of different lifestyles (mean values were subjected to bootstraps and rarefaction; colour key same as panel c). (b) Body size disparity (sum of variances) of different lifestyles (disparity values were subjected to bootstraps and rarefaction; colour key same as panel c). (c) Through‐time variation of body size (mean values per time bin) for different lifestyles. Data for time bins with only one species are not displayed. Source: Data from Godoy PL, Benson RB, Bronzati M and Butler RJ () The multi‐peak adaptive landscape of crocodylomorph body size evolution. BMC Evolutionary Biology 19: 167.
Figure 5. Body size patterns of crocodylians. Body size is represented by a cranial measurement (dorsal orbito‐cranial length) after log‐transformation. (a) Mean body size (green line) through time, plotted with environmental temperature data (red line). Temperature is represented by δ18O data (lower values indicate higher temperatures). (b) Mean body size regressed against temperature, indicating a strong correlation (significant coefficient of determination (R2) = 0.828). (c) Through‐time variation of crocodylian latitudinal distribution. Body size is incorporated into the plot as different‐sized circles. Latitude values are absolute (i.e. without distinction between north and south). For extant crocodylians, maximum latitudinal range was considered. Sources: Godoy PL, Benson RB, Bronzati M and Butler RJ () The multi‐peak adaptive landscape of crocodylomorph body size evolution. BMC Evolutionary Biology 19: 167; Zachos JC, Dickens GR and Zeebe RE () An early Cenozoic perspective on greenhouse warming and carbon‐cycle dynamics. Nature 451: 279–283.
close

References

Allen BJ, Stubbs TL, Benton MJ and Puttick MN (2019) Archosauromorph extinction selectivity during the Triassic–Jurassic mass extinction. Palaeontology 62: 211–224.

Allsteadt J and Lang JW (1995) Incubation temperature affects body size and energy reserves of hatchling American alligators (Alligator mississippiensis). Physiological Zoology 68: 76–97.

Aureliano T, Ghilardi AM, Guilherme E, et al. (2015) Morphometry, bite‐force, and paleobiology of the Late Miocene caiman Purussaurus brasiliensis. PLoS One 10: e0117944.

Benton MJ and Clark JM (1988) Archosaur phylogeny and the relationships of the Crocodylia. In: Benton MJ (ed.) The Phylogeny and Classification of the Tetrapods, pp 295–338. Clarendon Press: Oxford.

Brochu CA (2010) A new alligatorid from the lower Eocene Green River Formation of Wyoming and the origin of caimans. Journal of Vertebrate Paleontology 30: 1109–1126.

Brochu CA and Sumrall CD (2020) Modern cryptic species and crocodylian diversity in the fossil record. Zoological Journal of the Linnean Society. DOI: 10.1093/zoolinnean/zlaa039.

Bronzati M, Montefeltro FC and Langer MC (2015) Diversification events and the effects of mass extinctions on Crocodyliformes evolutionary history. Royal Society Open Science 2: 140385.

Cidade GM, Riff D and Hsiou AS (2019) The feeding habits of the strange crocodylian Mourasuchus (Alligatoroidea, Caimaninae): a review, new hypotheses and perspectives. Revista Brasileira de Paleontologia 22: 106–119.

Clark JM (2011) A new shartegosuchid crocodyliform from the Upper Jurassic Morrison Formation of western Colorado. Zoological Journal of the Linnean Society 163: S152–S172.

Clauset A and Erwin DH (2008) The evolution and distribution of species body size. Science 321: 399–401.

de Celis A, Narváez I and Ortega F (2019) Spatiotemporal palaeodiversity patterns of modern crocodiles (Crocodyliformes: Eusuchia). Zoological Journal of the Linnean Society. DOI: 10.1093/zoolinnean/zlz038.

Farlow JO, Hurlburt GR, Elsey RM, Britton AR and Langston W (2005) Femoral dimensions and body size of Alligator mississippiensis: estimating the size of extinct mesoeucrocodylians. Journal of Vertebrate Paleontology 25: 354–369.

Felsenstein J (1985) Phylogenies and the comparative method. The American Naturalist 125: 1–15.

Fernández M and Gasparini Z (2008) Salt glands in the Jurassic metriorhynchid Geosaurus: implications for the evolution of osmoregulation in Mesozoic marine crocodyliforms. Naturwissenschaften 95: 79–84.

Gaston KJ (2000) Global patterns in biodiversity. Nature 405: 220–227.

Gearty W and Payne JL (2020) Physiological constraints on body size distributions in Crocodyliformes. Evolution 74: 245–255.

Godoy PL, Ferreira GS, Montefeltro FC, et al. (2018) Evidence for heterochrony in the cranial evolution of fossil crocodyliforms. Palaeontology 61: 543–558.

Godoy PL, Benson RB, Bronzati M and Butler RJ (2019) The multi‐peak adaptive landscape of crocodylomorph body size evolution. BMC Evolutionary Biology 19: 167.

Godoy PL (2020) Crocodylomorph cranial shape evolution and its relationship with body size and ecology. Journal of Evolutionary Biology 33: 4–21.

Hansen TF (1997) Stabilizing selection and the comparative analysis of adaptation. Evolution 51: 1341–1351.

Herrera Y, Fernandez MS, Lamas SG, et al. (2017) Morphology of the sacral region and reproductive strategies of Metriorhynchidae: a counter‐inductive approach. Earth and Environmental Science Transactions of the Royal Society of Edinburgh 106: 247–255.

Hunt G and Slater G (2016) Integrating paleontological and phylogenetic approaches to macroevolution. Annual Review of Ecology, Evolution, and Systematics 47: 189–213.

Irmis RB, Nesbitt SJ and Sues HD (2013) Early Crocodylomorpha. In: Nesbitt SJ, Desojo JB and Irmis RB (eds) Anatomy, Phylogeny and Palaeobiology of Early Archosaurs and their Kin, Special Publications 379, pp 275–302. Geological Society of London: London.

Jetz W, Thomas GH, Joy JB, Hartmann K and Mooers AO (2012) The global diversity of birds in space and time. Nature 491: 444–448.

Lakin RJ, Barrett PM, Stevenson C, Thomas RJ and Wills MA (2020) First evidence for a latitudinal body mass effect in extant Crocodylia and the relationships of their reproductive characters. Biological Journal of the Linnean Society 129: 875–887.

Longrich NR, Bhullar BAS and Gauthier JA (2012) Mass extinction of lizards and snakes at the Cretaceous–Paleogene boundary. Proceedings of the National Academy of Sciences 109: 21396–21401.

Louca S and Pennell MW (2020) Extant timetrees are consistent with a myriad of diversification histories. Nature 580: 502–505.

Lyson TR, Miller IM, Bercovici AD, et al. (2019) Exceptional continental record of biotic recovery after the Cretaceous–Paleogene mass extinction. Science 366: 977–983.

Mannion PD, Benson RB, Carrano MT, et al. (2015) Climate constrains the evolutionary history and biodiversity of crocodylians. Nature Communications 6: 1–9.

Mannion PD, Chiarenza AA, Godoy PL and Cheah YN (2019) Spatiotemporal sampling patterns in the 230 million year fossil record of terrestrial crocodylomorphs and their impact on diversity. Palaeontology 62: 615–637.

Markwick PJ (1998a) Fossil crocodilians as indicators of Late Cretaceous and Cenozoic climates: implications for using palaeontological data in reconstructing palaeoclimate. Palaeogeography, Palaeoclimatology, Palaeoecology 137: 205–271.

Markwick PJ (1998b) Crocodilian diversity in space and time: the role of climate in paleoecology and its implication for understanding K/T extinctions. Paleobiology 24: 470–497.

McKinney ML (1990) Trends in body size evolution. In: McNamara KJ (ed.) Evolutionary Trends, pp 75–118. University of Arizona Press: Tucson.

Melstrom KM and Irmis RB (2019) Repeated evolution of herbivorous crocodyliforms during the age of dinosaurs. Current Biology 29: 2389–2395.

Nicolaï MP and Matzke NJ (2019) Trait‐based range expansion aided in the global radiation of Crocodylidae. Global Ecology and Biogeography 28: 1244–1258.

O'Brien HD, Lynch LM, Vliet KA, et al. (2019) Crocodylian head width allometry and phylogenetic prediction of body size in extinct crocodyliforms. Integrative Organismal Biology 1: obz006.

Pigot AL, Sheard C, Miller ET, et al. (2020) Macroevolutionary convergence connects morphological form to ecological function in birds. Nature Ecology & Evolution 4: 230–239.

Salas‐Gismondi R, Flynn JJ, Baby P, et al. (2016) A new 13 million year old gavialoid crocodylian from proto‐Amazonian mega‐wetlands reveals parallel evolutionary trends in skull shape linked to longirostry. PLoS One 11: e0152453.

Seymour RS, Bennett‐Stamper CL, Johnston SD, Carrier DR and Grigg GC (2004) Evidence for endothermic ancestors of crocodiles at the stem of archosaur evolution. Physiological and Biochemical Zoology 77: 1051–1067.

Seymour RS, Gienger CM, Brien ML, et al. (2013) Scaling of standard metabolic rate in estuarine crocodiles Crocodylus porosus. Journal of Comparative Physiology B 183: 491–500.

Schmidt‐Nielsen K (1984) Scaling: Why is Animal Size so Important? Cambridge University Press: Cambridge.

Schwarz D, Raddatz M and Wings O (2017) Knoetschkesuchus langenbergensis gen. nov. sp. nov., a new atoposaurid crocodyliform from the Upper Jurassic Langenberg Quarry (Lower Saxony, northwestern Germany), and its relationships to Theriosuchus. PLoS One 12: e0160617.

Smith EN (1976) Heating and cooling rates of the American alligator, Alligator mississippiensis. Physiological Zoology 49: 37–48.

Solórzano A, Núñez‐Flores M, Inostroza‐Michael O and Hernández CE (2019) Biotic and abiotic factors driving the diversification dynamics of Crocodylia. Palaeontology 63: 415–429.

Stanley SM (1973) An explanation for Cope's rule. Evolution 27: 1–26.

Turner AH and Nesbitt SJ (2013) Body size evolution during the Triassic archosauriform radiation. In: Nesbitt SJ, Desojo JB and Irmis RB (eds) Anatomy, Phylogeny and Palaeobiology of Early Archosaurs and their Kin, Special Publications 379, pp 573–597. Geological Society of London: London.

Turner AH, Pritchard AC and Matzke NJ (2017) Empirical and Bayesian approaches to fossil‐only divergence times: a study across three reptile clades. PLoS One 12: e0169885.

Wilberg EW, Turner AH and Brochu CA (2019) Evolutionary structure and timing of major habitat shifts in Crocodylomorpha. Scientific Reports 9: 514.

Young MT, Rabi M, Bell MA, et al. (2016) Big‐headed marine crocodyliforms and why we must be cautious when using extant species as body length proxies for long‐extinct relatives. Palaeontologia Electronica 19: 1–14.

Zachos JC, Dickens GR and Zeebe RE (2008) An early Cenozoic perspective on greenhouse warming and carbon‐cycle dynamics. Nature 451: 279–283.

Further Reading

Benson RB and Godoy PL (2019) Evolution: much on the menu for ancient crocs. Current Biology 29: R683–R685.

Butler MA and King AA (2004) Phylogenetic comparative analysis: a modeling approach for adaptive evolution. The American Naturalist 164: 683–695.

Grigg G and Kirshner D (2015) Biology and Evolution of Crocodylians. Cornell University Press: New York.

Hansen TF (2012) Adaptive landscapes and macroevolutionary dynamics. In: Svensson E and Calsbeek R (eds) The Adaptive Landscape in Evolutionary Biology, pp 205–226. Oxford University Press: Oxford.

Hunt G and Carrano MT (2010) Models and methods for analyzing phenotypic evolution in lineages and clades. The Paleontological Society Papers 16: 245–269.

Peters RH (1983) The Ecological Implications of Body Size. Cambridge University Press: New York.

Pol D and Leardi JM (2015) Diversity patterns of Notosuchia (Crocodyliformes, Mesoeucrocodylia) during the Cretaceous of Gondwana. In: Fernández M and Herrera Y (eds) Reptiles Extintos – Volumen en Homenaje a Zulma Gasparini, pp 172–186. Publicación Electrónica de la Asociación Paleontológica Argentina: Buenos Aires.

Simpson GG (1944) Tempo and Mode in Evolution. Columbia University Press: New York.

Simpson GG (1953) Major Features of Evolution. Columbia University Press: New York.

Slavenko A, Tallowin OJ, Itescu Y, Raia P and Meiri S (2016) Late Quaternary reptile extinctions: size matters, insularity dominates. Global Ecology and Biogeography 25: 1308–1320.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Godoy, Pedro L, and Turner, Alan H(Oct 2020) Body Size Evolution in Crocodylians and Their Extinct Relatives. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0029089]