Integrated diversification of locomotion and feeding in labrid fishes

Abstract

An organism's performance of any ecological task involves coordination of multiple functional systems. Feeding performance is influenced by locomotor abilities which are used during search and capture of prey, as well as cranial mechanics, which affect prey capture and processing. But, does this integration of functional systems manifest itself during evolution? We asked whether the locomotor and feeding systems evolved in association in one of the most prominent and diverse reef fish radiations, the Labridae. We examined features of the pectoral fins that affect swimming performance and aspects of the skull that describe force and motion of the jaws. We applied a recent phylogeny, calculated independent contrasts for 60 nodes and performed principal components analyses separately on contrasts for fin and skull traits. The major axes of fin and skull diversification are highly correlated; modifications of the skull to amplify the speed of jaw movements are correlated with changes in the pectoral fins that increase swimming speed, and increases in force capacity of the skull are associated with changes towards fins that produce high thrust at slow speeds. These results indicate that the labrid radiation involved a strong connection between locomotion and feeding abilities.

Figure 1

(a) Labrid pectoral fins vary in AR, including low AR forms, as in Labropsis australis (southern tubelip) and high AR forms, as in Gomphosus varius (bird wrasse). Species with high AR fins typically employ a flapping stroke during swimming, which is reflected in the shallow angle of attachment between the fin (oblique, dashed line) and the long axis of the body (horizontal, dashed line). Species with low AR fins use a rowing fin stroke, associated with a deep angle of attachment. (b) Labrid skull morphology varies between forceful jaws, as in Choerodon anchorago (orange-dotted tuskfish), and jaws that amplify velocity, as seen in Clepticus parrae (creole wrasse). The morphological differences between species depicted in (a,b) reflect the principal axes of pectoral fin and skull evolution, respectively.

Figure 2

Plot of pectoral fin PC 1 and skull PC 1. Points are PC scores for 60 internal nodes of the labrid phylogeny and were derived from PCA on independent contrasts for pectoral fin and cranial traits. Fin PC 1 explains 80% of the total variation in fin contrasts and skull PC 1 accounts for 30% of the total variation in skull contrasts. Variables with significant PC loadings are shown on each axis, and arrows indicate their directions. These two primary axes of locomotor and cranial diversification are significantly correlated (r=−0.53; p<0.001).