Computational Fluid Dynamics Suggests Ecological Diversification among Stem-Gnathostomes

Abstract

The evolutionary assembly of the vertebrate bodyplan has been characterised as a longterm ecological trend towards increasingly active and predatory lifestyles, culminating in jawed vertebrates which dominate modern vertebrate biodiversity [1-8]. This contrast is no more stark than between the earliest jawed vertebrates and their immediate relatives, the extinct jawless, dermal armour-encased osteostracans, which have conventionally been interpreted as benthic mud-grubbers with poor swimming capabilities, and low manoeuvrability [9-12]. 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 [9-12] with the origin of jaws as the key innovation that precipitated the ecological diversification of the group [13,14]. RESULTSThe origin of vertebrates can be characterised by increased cephalisation and a number of developmental and anatomical innovations rooted in whole genome duplication, increased

Functional assessment of morphological homoplasy in stem-gnathostomes

“…We used geometric morphometrics to numerically describe the morphological diversity of osteostracan and galeaspid headshields following Ferrón et al [14,15]. Landmark digitization was performed on photographic images of specimens from Ferrón et al [15] and Zhu [12] using TpsDig v.2.26 [16] (electronic supplementary material, table S1).…”

“…The resulting three-dimensional models were scaled to life size using Netfabb Basic and converted into NURBS surfaces in Geomagic Studio (www.geomagic.com). Osteostracan models correspond to those used in Ferrón et al [14].…”

“…Computational fluid dynamics is a computational method for simulating fluid flow (liquids or gases) and their interaction with solid surfaces, enabling large-scale comparative analyses for resolving functional and ecological hypotheses in extinct taxa [38]. We performed simulations of water flow around the three-dimensional models in COMSOL Multiphysics 5.2 (http://www.comsol.com), following the procedure outlined in Ferrón et al [14]. Pelagic and benthic conditions were emulated in order to assess the functional constraints of homoplasy in different ecological scenarios.…”

“…We performed simulations of water flow around the threedimensional models in COMSOL Multiphysics 5.2 (http://www. comsol.com), following the procedure outlined in Ferrón et al [11]. Pelagic and benthic conditions were emulated in order to assess the functional constraints of homoplasy in different ecological scenarios.…”

“…Indeed, the bodyplans of osteostracans and galeaspids exhibit gross similarity [9] (figure 1a), including bony headshields that have similar cephalic elaborations (elongated rostra, lateral expansions or processes) and vary between oblate and prolate cephalic profiles [10][11][12][13]. Ferrón et al [14] showed that in osteostracans these structures represent adaptations for passive hydrodynamic control, including lift generation. Here, we attempt to provide insight into the ecology of the gnathostome ancestor by characterising quantitatively similarities in the anatomy of galeaspids and osteostracans and, through computational fluid dynamics (CFD), determine whether these similarities have a common functional basis.…”