Decoupled diversification dynamics of feeding morphology following a major functional innovation in marine butterflyfishes

Abstract

The diversity of fishes on coral reefs is influenced by the evolution of feeding innovations. For instance, the evolution of an intramandibular jaw joint has aided shifts to corallivory in Chaetodon butterflyfishes following their Miocene colonization of coral reefs. Today, over half of all Chaetodon species consume coral, easily the largest concentration of corallivores in any reef fish family. In contrast with Chaetodon, other chaetodontids, including the long-jawed bannerfishes, remain less intimately associated with coral and mainly consume other invertebrate prey. Here, we test (i) if intramandibular joint (IMJ) evolution in Chaetodon has accelerated feeding morphological diversification, and (ii) if cranial and post-cranial traits were affected similarly. We measured 19 cranial functional morphological traits, gut length and body elongation for 33 Indo-Pacific species. Comparisons of Brownian motion rate parameters revealed that cranial diversification was about four times slower in Chaetodon butterflyfishes with the IMJ than in other chaetodontids. However, the rate of gut length evolution was significantly faster in Chaetodon, with no group-differences for body elongation. The contrasting patterns of cranial and post-cranial morphological evolution stress the importance of comprehensive datasets in ecomorphology. The IMJ appears to enhance coral feeding ability in Chaetodon and represents a design breakthrough that facilitates this trophic strategy. Meanwhile, variation in gut anatomy probably reflects diversity in how coral tissues are procured and assimilated. Bannerfishes, by contrast, retain a relatively unspecialized gut for processing invertebrate prey, but have evolved some of the most extreme cranial mechanical innovations among bony fishes for procuring elusive prey.

Keywords: Chaetodontidae; biting feeding mode; design breakthrough; ecological threshold; functional disparity; key innovation.

Figure 1.

Phylomorphospace for the Chaetodontidae with PC1 versus PC2 and the phylogeny (grey lines) superimposed, using the phylomorphospace function in Phytools [43]. Names are given for species depicted and subfamily status is shown by colour (blue, butterflyfishes; red, bannerfishes). The main axis of morphological variation within the family is highlighted by representative tooth-bearing jaw bones (pmx, premaxillary; d, dentary) adjacent to their bearers.

Figure 2.

Maximum clade credibility phylogeny generated using the data, methods and calibration points from Bellwood et al. [26]. Dietary groups (adapted from [26]) are indicated by capital letters. Coloured circles at the branch tips indicate the value of PC1 for each species, which describes a gradient of jaw lengths (see heat-map) from short (C. ornatissimus) to long (Forcipiger flavissimus). Coloured squares indicate the value of relative gut index (gut length divided by orbital standard length (OSL)), ranging from 0.4 in Hemitaurichthys thompsoni to 21.1 in C. ornatissimus.