Diversification of axial body plan and its underlying developmental mechanisms in a clade of extinct marine reptiles

Understanding how developmental processes change on macroevolutionary timescales to generate body plan diversity is fundamental to the study of vertebrate evolution. In this study we highlight that the application of phylogenetic comparative methods to extinct clades can complement results from living groups, to shed light on the macroevolutionary dynamics of morphology, and its underlying developmental mechanisms, particularly on very long timescales. Sauropterygian marine reptiles (nothosaurs, plesiosaurs, pliosaurs and kin) have long been the focus of qualitative hypotheses about the evolution of body plan, and its relationship with ecological niche occupation. Early taxonomy of the Jurassic-Cretaceous members of this clade classified taxa into two groups corresponding to their gross axial body plan morphologies: ‘plesiosaurs’ characterised by long necks, small skulls and short trunks, and ‘pliosaurs’ characterised by short necks, large skulls and long trunks; these have since been shown not to represent clades. Recently developed phylogenetic comparative methods, applied to trees of fossil taxa, offer an opportunity to quantitatively assess long-standing qualitative hypotheses. Here we use two heterogeneous phylogenetic modelling approaches – AUTEUR and the general FPK model - applied to a comprehensive phylogeny of Sauropterygia. We show that change in relative neck length was primarily enabled by homeotic shifts, with a lesser but important contribution from post-patterning growth, and is best modelled by constant rate Brownian motion. This is in contrast to relative skull size, which is best modelled by a two-peak adaptive landscape. Both of these contradict the traditional hypothesis of long-term divergent trends, beginning in the Middle Triassic. In combination with our other recent work this demonstrates that the apparent Sauropterygian body plan dichotomy resulted from ancestrally high evolutionary plasticity, which was subsequently maintained, and a complex evolutionary history and pattern of ecological diversification.