Computational fluid dynamics suggests ecological diversification among stem-gnathostomes

The evolutionary assembly of the vertebrate bodyplan has been characterized as a long-term ecological trend toward increasingly active and predatory lifestyles, culminating in jawed vertebrates that dominate modern vertebrate biodiversity [1, 2, 3, 4, 5, 6, 7, 8]. This contrast is no more stark than between the earliest jawed vertebrates and their immediate relatives, the extinct jawless, dermal armor-encased osteostracans, which have conventionally been interpreted as benthic mud-grubbers with poor swimming capabilities and low maneuverability [9, 10, 11, 12]. Using computational fluid dynamics, we show that osteostracan headshield morphology is compatible with a diversity of hydrodynamic efficiencies including passive control of water flow around the body; these could have increased versatility for adopting diverse locomotor strategies. Hydrodynamic performance varies with morphology, proximity to the substrate, and angle of attack (inclination). Morphotypes with dorsoventrally oblate headshields are hydrodynamically more efficient when swimming close to the substrate, whereas those with dorsoventrally more prolate headshields exhibit maximum hydrodynamic efficiency when swimming free from substrate effects. These results suggest different hydrofoil functions among osteostracan headshield morphologies, compatible with ecological diversification and undermining the traditional view that jawless stem-gnathostomes were ecologically constrained [9, 10, 11, 12] with the origin of jaws as the key innovation that precipitated the ecological diversification of the group [13, 14]

Functional assessment of morphological homoplasy in stem-gnathostomes

Osteostraci and Galeaspida are stem-gnathostomes, occupying a key phylogenetic position for resolving the nature of the jawless ancestor from which jawed vertebrates evolved more than 400 million years ago. Both groups are characterized by the presence of rigid headshields that share a number of common morphological traits, in some cases hindering the resolution of their interrelationships and the exact nature of their affinities with jawed vertebrates. Here, we explore the morphological and functional diversity of osteostracan and galeaspid headshields using geometric morphometrics and computational fluid dynamics to constrain the factors that promoted the evolution of their similar morphologies and informing on the ecological scenario under which jawed vertebrates emerged. Phylomorphospace, Mantel analysis and Stayton metrics demonstrate a high degree of homoplasy. Computational fluid dynamics reveals similar hydrodynamic performance among morphologically convergent species, indicating the independent acquisition of the same morphofunctional traits and, potentially, equivalent lifestyles. These results confirm that a number of the characters typically used to infer the evolutionary relationships among galeaspids, osteostracans and jawed vertebrates are convergent in nature, potentially obscuring understanding of the assembly of the gnathostome bodyplan. Ultimately, our results reveal that while the jawless relatives of the earliest jawed vertebrates were ecologically diverse, widespread convergence on the same hydrodynamic adaptations suggests they had reached the limits of their potential ecological diversity—overcome by jawed vertebrates and their later innovations