Functional adaptive landscapes predict terrestrial capacity at the origin of limbs

Abstract

The acquisition of terrestrial, limb-based locomotion during tetrapod evolution has remained a subject of debate for more than a century1,2. Our current understanding of the locomotor transition from water-to-land is largely based on a few exemplar fossils such as Tiktaalik3, Acanthostega4, Ichthyostega5, and Pederpes6. However, isolated bony elements may reveal hidden functional diversity, providing a more comprehensive evolutionary perspective7. Here we analyse 40 three-dimensional tetrapodomorph humeri spanning the fin-to-limb transition and use functionally-informed ecological adaptive landscapes8–10 to reconstruct the evolution of terrestrial locomotion. We show that humerus shape change is driven by ecology and phylogeny and is associated with functional trade-offs related to locomotor performance. Two divergent adaptive landscapes are recovered for aquatic fishes and terrestrial crown tetrapods, each defined by a different combination of functional specialisations. Stem tetrapod humeri share a unique suite of functional adaptations, but do not conform to their own predicted adaptive peak. Instead, stem tetrapod humeri fall at the base of the crown tetrapod landscape, indicating the capacity for terrestrial locomotion with the origin of limbs. Our results suggest that stem tetrapods utilised transitional gaits5,11 during the initial stages of land exploration, stabilised by the opposing selective pressures of their amphibious habits. Effective limb-based locomotion did not arise until loss of the ancestral ‘L-shaped’ humerus in the crown group, setting the stage for diversification of terrestrial tetrapods and establishment of modern ecological niches12,13.