Evolutionary rate incongruences in squamates reveal contrasting patterns of evolutionary novelties and innovation

Tiago Simoes , Arthur S. Brum, Stephanie E. Pierce

Understanding the rate of phenotypic evolution can reveal fundamental aspects of organismal evolutionary trajectories. Hence, several studies have attempted to detect the tempo of evolution for multiple organisms, although based on radically different datatypes (e.g., discrete and morphometric) and methods (phylodynamic vs comparative methods). Here, we ask whether these competing approaches provide comparable rate trajectories using an expanded squamate phylogenetic dataset that is matched (to the species-level) with new geometric morphometric data, while also assessing method robustness to fossil sampling. Our new squamate total-evidence time-tree suggests a new placement for putative stem iguanians while matching divergence time estimates of recent phylogenomic studies. We show that low fossil sampling inadvertently removes entire regions of the morphospace and contraction of crown clade phenotypic diversity, as morphospace boundaries are frequently delimited by transitional fossils. Critically, different datatypes produce radically incongruent rate patterns, which are further exacerbated by methodological differences. We suggest that phylogenetic discrete data (i.e., characters) are strongly influenced by neomorphisms and reveal phenotypic novelties, while morphometric data (i.e., shape) reflects changes in phenotypic refinement leading to phenotypic innovation. This conceptual distinction conciliates discrepant macroevolution trajectories across squamates, which we expect to be generalizable to other systems across the Tree of Life.