The multi-peak adaptive landscape of crocodylomorph body size evolution

Abstract

Background Little is known about the long-term patterns of body size evolution in Crocodylomorpha, the > 200-million-year-old group that includes living crocodylians and their extinct relatives. Extant crocodylians are mostly large-bodied (3–7 m) predators. However, extinct crocodylomorphs exhibit a wider range of phenotypes, and many of the earliest taxa were much smaller (< 1.2 m). This suggests a pattern of size increase through time that could be caused by multi-lineage evolutionary trends of size increase or by selective extinction of small-bodied species. Here, we characterise patterns of crocodylomorph body size evolution using a model fitting-approach (with cranial measurements serving as proxies). We also estimate body size disparity through time and quantitatively test hypotheses of biotic and abiotic factors as potential drivers of crocodylomorph body size evolution. Results Crocodylomorphs reached an early peak in body size disparity during the Late Jurassic, and underwent an essentially continual decline since then. A multi-peak Ornstein-Uhlenbeck model outperforms all other evolutionary models fitted to our data (including both uniform and non-uniform), indicating that the macroevolutionary dynamics of crocodylomorph body size are better described within the concept of an adaptive landscape, with most body size variation emerging after shifts to new macroevolutionary regimes (analogous to adaptive zones). We did not find support for a consistent evolutionary trend towards larger sizes among lineages (i.e., Cope’s rule), or strong correlations of body size with climate. Instead, the intermediate to large body sizes of some crocodylomorphs are better explained by group-specific adaptations. In particular, the evolution of a more aquatic lifestyle (especially marine) correlates with increases in average body size, though not without exceptions. Conclusions Shifts between macroevolutionary regimes provide a better explanation of crocodylomorph body size evolution on large phylogenetic and temporal scales, suggesting a central role for lineage-specific adaptations rather than climatic forcing. Shifts leading to larger body sizes occurred in most aquatic and semi-aquatic groups. This, combined with extinctions of groups occupying smaller body size regimes (particularly during the Late Cretaceous and Cenozoic), gave rise to the upward-shifted body size distribution of extant crocodylomorphs compared to their smaller-bodied terrestrial ancestors. Electronic supplementary material The online version of this article (10.1186/s12862-019-1466-4) contains supplementary material, which is available to authorized users.

Physiological constraints on body size distributions in Crocodyliformes

“…The evolution of crocodyliform body size cannot be reconciled with a simple Brownian motion model (Godoy et al. ). Rather, the best model of body size evolution is one in which the adaptive landscape contains many unique optimal body sizes.…”

“…Specifically, shifts to larger sizes are often linked to more aquatic lifestyles (Godoy et al. ). However, it has yet to be determined what selective pressure(s) caused these independent size shifts that are associated with living in water.…”

Biotic and abiotic factors driving the diversification dynamics of Crocodylia

“…Important aspects of crocodylomorph body size evolution can be revealed by calculating body size disparity through time; for example, the degree of similarity in body size among species typically reflects the strength of resource competition (Godoy et al . ). The BM of each taxon was transformed into a logarithmic scale to better represent proportional changes in body mass, and to reduce potential bias (Lyons & Smith ).…”

“…; Godoy et al . ). Despite this, the relevance of biotic forces, such as morphological disparity (e.g.…”

“…This is intriguing because: (1) body mass influences the way in which animals interact with their environment (Lyons & Smith ); (2) the degree of similarity in body size among species typically reflects the strength of resource competition (Godoy et al . ); and (3) both extant and extinct crocodylian show a large disparity of body sizes (Schwimmer ; Trutnau & Sommerlad ; Riff & Aguilera ; Aureliano et al . ; Grigg ; Godoy et al .…”