Evolutionary structure and timing of major habitat shifts in Crocodylomorpha

Abstract

Extant crocodylomorphs are semiaquatic ambush predators largely restricted to freshwater or estuarine environments, but the group is ancestrally terrestrial and inhabited a variety of ecosystems in the past. Despite its rich ecological history, little effort has focused on elucidating the historical pattern of ecological transitions in the group. Traditional views suggested a single shift from terrestrial to aquatic in the Early Jurassic. However, new fossil discoveries and phylogenetic analyses tend to imply a multiple-shift model. Here we estimate ancestral habitats across a comprehensive phylogeny and show at least three independent shifts from terrestrial to aquatic and numerous other habitat transitions. Neosuchians first invade freshwater habitats in the Jurassic, with up to four subsequent shifts into the marine realm. Thalattosuchians first appear in marine habitats in the Early Jurassic. Freshwater semiaquatic mahajangasuchids are derived from otherwise terrestrial notosuchians. Within nearly all marine groups, some species return to freshwater environments. Only twice have crocodylomorphs reverted from aquatic to terrestrial habitats, both within the crown group. All living non-alligatorid crocodylians have a keratinised tongue with salt-excreting glands, but the lack of osteological correlates for these adaptations complicates pinpointing their evolutionary origin or loss. Based on the pattern of transitions to the marine realm, our analysis suggests at least four independent origins of saltwater tolerance in Crocodylomorpha.

Figure 1

Traditional hypotheses of crocodylomorph habitat transition underpinning the single-shift model. (a) The “fertile Stamm” – a freshwater, semiaquatic phylogenetic core from which multiple lineages independently shift to terrestrial or marine ecosystems (adapted from ref.). (b) Spindle diagram of Langston, depicting a single shift to the aquatic realm from “Protosuchia” to “Mesosuchia” in the Early Jurassic (adapted from ref.). Green represents terrestrial habitats, gray/black represents freshwater semiaquatic, blue represents marine.

Figure 2

Phylogenetic and temporal pattern of habitat shifts within Crocodylomorpha. Colored arrows within circles indicate habitat transitions. Horizontal arrows indicate habitat transitions that occurred within collapsed groups. Combined green and black coloring of Calsoyasuchus represents uncertainty regarding its assigned habitat. Note that internal branches are scaled to make the figure legible, not according to the chronograms we employed in the analysis.

Figure 3

Phylogenetic and temporal pattern of habitat shifts within Thalattosuchia. Colored arrows within circles indicate habitat transitions. Ancestral state reconstructions at all nodes >0.9 in favor of one habitat. Note that internal branches are scaled to make the figure legible, not according to the chronograms we employed in the analysis.

Figure 4

Phylogenetic and temporal pattern of habitat shifts within Tethysuchia. Colored arrows within circles indicate habitat transitions. Pie chart at Dyrosauridae node indicates relative support for each habitat (shown only for nodes where ancestral state is reconstructed with a likelihood <0.9). Note that internal branches are scaled to make the figure legible, not according to the chronograms we employed in the analysis.

Figure 5

Phylogenetic and temporal pattern of habitat shifts within Crocodylia. Colored arrows within circles indicate habitat transitions. Ancestral state reconstructions at all nodes >0.9 in favor of one habitat. Note that internal branches are scaled to make the figure legible, not according to the chronograms we employed in the analysis.

Figure 6

Phylogenetic and temporal pattern of habitat shifts within Notosuchia. Colored arrows within circles indicate habitat transitions. Pie chart at basal node indicates relative support for each habitat (shown only for nodes where ancestral state is reconstructed with a likelihood <0.9). Note that internal branches are scaled to make the figure legible, not according to the chronograms we employed in the analysis.