Whole-body variational modularity in the zebrafish: an inside-out story of a model species

Abstract

Actinopterygians are the most diversified clade of extant vertebrates. Their impressive morphological disparity bears witness to tremendous ecological diversity. Modularity, the organization of biological systems into quasi-independent anatomical/morphological units, is thought to increase evolvability of organisms and facilitate morphological diversification. Our study aims to quantify patterns of variational modularity in a model actinopterygian, the zebrafish (Danio rerio), using three-dimensional geometric morphometrics on osteological structures isolated from micro-CT scans. A total of 72 landmarks were digitized along cranial and postcranial ossified regions of 30 adult zebrafishes. Two methods were used to test modularity hypotheses, the covariance ratio and the distance matrix approach. We find strong support for two modules, one comprised paired fins and the other comprised median fins, that are best explained by functional properties of subcarangiform swimming. While the skull is tightly integrated with the rest of the body, its intrinsic integration is relatively weak supporting previous findings that the fish skull is a modular structure. Our results provide additional support for the recognition of similar hypotheses of modularity identified based on external morphology in various teleosts, and at least two variational modules are proposed. Thus, our results hint at the possibility that internal and external modularity patterns may be congruent.

Keywords: functional integration; modularity; osteology; ray-finned fishes; three-dimensional geometric morphometrics; variational modularity.

Figure 1.

(a) Danio rerio specimen micro-CT-scanned showing the landmarks (yellow) positioning scheme. See electronic supplementary material, table S1 for complete description of the landmarks. (b) Graphical representation of the seven a priori hypotheses of modularity. Parts of the same colour belong to the same hypothetical variational module. See electronic supplementary material, table S3 for a complete description of the hypotheses.

Figure 2.

Network representations of the strengths of the relationships between modules based on pairwise comparisons of the CRs (a, c) and the PLS values (b, d). The thickness of the edges between vertices (i.e. modules) models the strength of integration.