Abstract
Understanding how developmental processes change on macroevolutionary timescales to generate body plan disparity is fundamental to the study of vertebrate evolution. Adult morphology of the vertebral column directly reflects the mechanisms that generate vertebral counts (somitogenesis) and their regionalisation (homeotic effects) during embryonic development. Sauropterygians were a group of Mesozoic marine reptiles that exhibited an extremely high disparity of presacral vertebral/somite counts. Using phylogenetic comparative methods, we demonstrate that somitogenesis and homeotic effects evolved in a co‐ordinated way among sauropterygians, contrasting with the wider pattern in tetrapods, in which somitogenetic and homeotic shifts are uncorrelated. Changes in sauropterygian body proportions were primarily enabled by homeotic shifts, with a lesser, but important, contribution from differences in postpatterning growth among somites. High body plan plasticity was present in Triassic sauropterygians and was maintained among their Jurassic and Cretaceous descendants. The extreme disparity in the body plan of plesiosaurian sauropterygians did not result from accelerated rates of evolutionary change in neck length, but instead reflect this ancestral versatility of sauropterygian axial development. Our results highlight variation in modes of axial development among tetrapods, and show that heterogeneous statistical models can uncover novel macroevolutionary patterns for animal body plans and the developmental mechanisms that control them.
Highlights
Sauropterygians are the longest persisting clade of secondarily aquatic tetrapods, with a time range spanning almost the entire duration of the Mesozoic (>180 million years [myr]; Motani 2009; Kelley and Pyenson 2015)
Based on ecomorphological traits such as tooth morphology and body proportions, it is likely that sauropterygians and other Mesozoic marine tetrapods filled some of the same niches as today’s marine mammals, and especially those of some odontocetes (Massare 1987; Collin and Janis 1997)
Rates of presacral count evolution are a proxy for evolutionary change in the number of somites generated during embryonic development
Summary
Sauropterygians are the longest persisting clade of secondarily aquatic tetrapods, with a time range spanning almost the entire duration of the Mesozoic (>180 million years [myr]; Motani 2009; Kelley and Pyenson 2015). Placodonts, the shortest necked sauropterygians, had necks comprising as few as six vertebrae and measuring as little as 14% of the trunk length (Rieppel 1995), whereas elasmosaurid plesiosaurians had as many as 76 cervical vertebrae and neck lengths nearly 400% of the trunk length (Kubo et al 2012) This high level of variation provides a model system for testing macroevolutionary hypotheses relating to vertebral development and body plan evolution in vertebrates, by quantifying patterns of evolutionary change in body proportions and vertebral counts in the context of a well-constrained phylogeny (Benson and Druckenmiller 2014; Jiang et al 2014)
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