Finite element and microstructural analyses indicate that pteraspid heterostracan oral plate microstructure was adapted to a mechanical function.

Abstract

Early vertebrate evolution has been characterized as a gradual shift from passive to more active feeding modes. However, this evolutionary scenario is contingent on poorly constrained inferences of the feeding ecology of extinct stem-gnathostomes. Heterostracans are among the earliest members of the gnathostome stem-lineage. Pteraspidiform heterostracans possessed an oral apparatus composed of rod-like plates that have been alternately interpreted to have been used for passive suspension feeding or mechanical food processing. Direct tests of the suspension feeding interpretation are challenging and so we tested hypotheses of a mechanical function using a combination of microstructural and finite element analysis (FEA). Our results demonstrate a negative relationship between simulated negative minimum principal stress (compressive stress) and bone volume fraction (a proxy for internal microstructure); the higher the stress, the higher the bone volume fraction. This relationship is clearest in the oral plate shaft. The hook, where the load is applied, shows the highest bone volume fraction values. Our results are compatible with adaption of skeletal microstructure to a mechanical function in which bone adaptively remodels under applied load to become denser to withstand increased stress. On this basis we reject the suspension feeding hypothesis in favour of a mechanical function for oral plates, such as deposit feeding or scavenging, in support for which we observe wear patterns on the aboral surface and the distal tip of the hook compatible with repeated abrasive polishing.