Ecological opportunity and the rise and fall of crocodylomorph evolutionary innovation

Abstract

Understanding the origin, expansion and loss of biodiversity is fundamental to evolutionary biology. The approximately 26 living species of crocodylomorphs (crocodiles, caimans, alligators and gharials) represent just a snapshot of the group's rich 230-million-year history, whereas the fossil record reveals a hidden past of great diversity and innovation, including ocean and land-dwelling forms, herbivores, omnivores and apex predators. In this macroevolutionary study of skull and jaw shape disparity, we show that crocodylomorph ecomorphological variation peaked in the Cretaceous, before declining in the Cenozoic, and the rise and fall of disparity was associated with great heterogeneity in evolutionary rates. Taxonomically diverse and ecologically divergent Mesozoic crocodylomorphs, like marine thalattosuchians and terrestrial notosuchians, rapidly evolved novel skull and jaw morphologies to fill specialized adaptive zones. Disparity in semi-aquatic predatory crocodylians, the only living crocodylomorph representatives, accumulated steadily, and they evolved more slowly for most of the last 80 million years, but despite their conservatism there is no evidence for long-term evolutionary stagnation. These complex evolutionary dynamics reflect ecological opportunities, that were readily exploited by some Mesozoic crocodylomorphs but more limited in Cenozoic crocodylians.

Rapid Initial Morphospace Expansion and Delayed Morphological Disparity Peak in the First 100 Million Years of the Archosauromorph Evolutionary Radiation

“…However, due to the poor sampling of pseudosuchian pelves in the Jurassic, this result should be treated with caution. However, this result agrees with conclusions of Toljagić and Butler (2013)-who investigated pseudosuchian disparity across the Triassic-Jurassic boundary based on discrete characters of the entire skeleton − that this extinction event affected primarily non-crocodylomorph pseudosuchians, while crocodylomorphs themselves radiated adaptively in the Early Jurassic, precipitating an increase in disparity and a shift in their morphospace occupation (see also Stubbs et al, 2021).…”

“…This indicates that disparity was not likely saturated by the end of the time span sampled here, and these trends of increase may continue in the Cretaceous. Similar delayed disparity peaks have been previously found for pterosaurs (Prentice et al, 2011;Butler et al, 2012;Foth et al, 2012), crocodylomorphs (Stubbs et al, 2021), and turtles (Foth and Joyce, 2016;Foth et al, 2017), but contrast with many smaller clades (see below). In contrast, concordant with our results for rates of change through time (see Discussion below), Archosauromorpha as a whole and all of the subclades examined (see specific points for Dinosauria, below) show broadly decreasing average displacement through time, indicating that evolutionary change tended to tail off after the initial radiation of novel ecomorphologies, concordant with an "early burst" pattern of evolution sensu lato (Puttick, 2018).…”

“…More surprisingly, the extension of the disparity analyses towards the end of the Jurassic reveals that after the decline in the Early Jurassic, the cranial disparity of pseudosuchians (represented by sum of variances) recovered in the Late Jurassic and surpassed that of avemetatarsalians. This increase in disparity is accompanied by a shift in morphospace and probably correlates with the adaptive radiation of crocodylomorphs in the Jurassic (Toljagić and Butler, 2013), when the clade radiated into a wide range of morphotypes with correspondingly varied cranial size and morphologies, including, for example, marine thalattosuchians, semi-aquatic goniopholidids, and terrestrial protosuchids (Bronzati et al, 2015;Mannion et al, 2015;Godoy et al, 2019;Stubbs et al, 2021). Only the terrestrial protosuchians were probably in direct competition with carnivorous avemetatarsalians, primarily small theropods.…”

Complex macroevolutionary dynamics underly the evolution of the crocodyliform skull

“…Explanations for these patterns may be derived from extrinsic or intrinsic factors, or both. Competition with mammals in the terrestrial and aquatic realms in the Cenozoic may have suppressed crocodyliforms from exploiting the same niches as their extinct relatives and limited them to the semi-aquatic niche that all living forms occupy [ 12 ]. Specialization to a specific habitat or niche itself can also create an evolutionary ratchet, limiting the ability to diversify into other niches, as is observed in mammalian hypercarnivores [ 43 ].…”

“…The crocodyliform skull shape is thought to vary primarily in the degree of snout (i.e. maxillary rostrum) elongation [4,5,[8][9][10][11][12]. Length and width of the snout are correlated with response to biomechanical stress and hydrodynamic properties and are thought to evolve in response to maximum prey size and other aspects of trophic ecology [8,9,11].…”