Evolutionary History and Taxonomic Reappraisal of Coral Reef Rabbitfishes (Siganidae): Patterns of Lineage Diversification and Speciation

SIMPLE SUMMARY: Herbivorous fish are recognized as being ecologically important to the health and survival of coral reef ecosystems because they remove algal turfs growing on corals. Apart from being one of the major components of herbivorous fish communities, rabbitfish are also characterized by possessing rabbit-like mouths. A total of 29 species of rabbitfish are confined to a single genus, Siganus, fish that are highly sought after for the aquarium trade and for food by humans. Natural hybridization between some species that have parapatric distributions across the Indo-West Pacific region may have homogenized their genotypic and morphological features. Relatively little is known, however, about how environmental factors may affect phylogenetic relationships among these siganid species. Based on sequencing of eight siganid species collected from the South China Sea and meta-analysis of sequences from ten siganid species retrieved from the NCBI database, we applied an integrated morphological–molecular approach to elucidate phylogenetic relationships and demographic histories of these species. Our results highlight that diversification and speciation of siganid species were influenced by a series of paleo-climatic events, changes to natural geographical distributions, and associated environmental changes. The target species were differentiated by body shape, and two morphometric parameters, notably body depth and snout length. Our results provide considerable baseline knowledge for strategizing improvement of both breeding and conservation programs for rabbitfish. ABSTRACT: Rabbitfish (Siganidae) are coral reef fish that are distributed across diverse habitats that include estuaries, mangroves, reefs, and even seaweed mats. Given their ecological diversity and natural widespread distributions across the Indo-Pacific region, we were interested to investigate the evolutionary history of this group and patterns of divergence that have contributed to their present-day distributions. In the present study, samples were collected from the South China Sea to study taxonomic and phylogenetic relationships, and divergence times. We investigated the taxonomic relationships among modern rabbitfish species, reconstructed their molecular phylogeny, and estimated divergence times among selected lineages based on a fragment of the mtDNA cytochrome oxidase I (COI) and sequences of the nuclear rhodopsin retrogene (RHO). Our results indicate that modern rabbitfish likely originated in the Indo-West Pacific during the late Eocene [37.4 million years ago (mya)], following which they diverged into three major clades during the Pliocene/Pleistocene. Subsequent diversification and origins of the majority of siganids may likely be associated with episodes of paleo-oceanographic events, including greenhouse and glaciation events (Eocene–Miocene) as well as major plate tectonic events (Pliocene–Pleistocene). Some modern siganid species may naturally hybridize with congeneric species where their geographical ranges overlap. A comprehensive taxonomic analysis revealed that the phylogeny of Siganidae (cladogenesis of Clades I, II, and III) is characterized by divergence in several external morphological characters and morphometric parameters. Our study demonstrates that morphological characteristics, geographical heterogeneity, and environmental change have contributed to siganids’ historical diversification.