Novel Tests of the Key Innovation Hypothesis: Adhesive Toepads in Arboreal Lizards

Abstract The evolution of key innovations—unique features that enable a
lineage to interact with the environment in a novel way—may drive broad
patterns of adaptive diversity. However, traditional tests of the key
innovation hypothesis, those which attempt to identify the evolutionary
effect of a purported key innovation by comparing patterns of diversity
between lineages with and without the key trait, have been challenged on
both conceptual and statistical grounds. Here, we explore alternative,
untested hypotheses of the key innovation framework. In lizards, adhesive
toepad structures increase grip strength on vertical and smooth surfaces
such as tree trunks and leaves and have independently evolved multiple
times. As such, toepads have been posited as a key innovation for the
evolution of arboreality. Leveraging a habitat use dataset applied to a
global phylogeny of 2692 lizard species, we estimated multiple origins of
toepads in three major clades and more than 100 origins of arboreality
widely across the phylogeny. Our results suggest that toepads arise
adaptively in arboreal lineages and are subsequently rarely lost while
maintaining arboreal ecologies. Padless lineages transition away from
arboreality at a higher rate than those with toepads, and high rates of
invasion of arboreal niches by non-arboreal padbearing lineages provides
further evidence that toepads may be a key to unlocking evolutionary
access to the arboreal zone. Our results and analytical framework provide
novel insights to understand and evaluate the ecological and evolutionary
consequences of key innovations.