Phylogeography of Heteropriacanthus, a circumtropical reef fish with very little morphological variation

Only six species of fishes found on reefs are known to have a circumtropical distribution. Until recently Heteropriacanthus cruentatus was one of the six, recognized as a single species in a monotypic genus present in all tropical and subtropical seas. Based on sequences of cytochrome oxidase I and on morphology, a previous study split the genus into three species, H. carolinus in the Indo-Pacific, H. cruentatus in most of the tropical Atlantic, and H. fulgens in the northeast Atlantic. We sampled two mitochondrial and three nuclear genes (a total of 3618 bases) from 21 locations in three oceans to determine the phylogeography and genetic structure of the genus. We found three clades, corresponding to H. cruentatus, H. fulgens, and H. carolinus. H. fulgens extends, not just to the northeastern Atlantic as previously known, but also to the southeast, the central and (possibly) the southwest Atlantic, whereas H. cruentatus is restricted to the Greater Caribbean. H. carolinus spreads in the entire Indo-Pacific. We found no evidence that the three species are sympatric anywhere in their range. H. cruentatus is genetically homogeneous over its small range, but H. fulgens shows evidence of gene flow restrictions between the northeast and the southeast Atlantic and between the east and the central Atlantic. Genetic exchange in H. carolinus is restricted by the large expanse of open water between the eastern and the central Pacific (the 4000 km wide Eastern Pacific Barrier), and by either distance or historical separation between the Pacific and the Indian Oceans. There is evidence of isolation by distance in H. carolinus, but not in H. fulgens or H. cruentatus. A coalescent Bayesian Analysis also supported a stepping stone model in H. carolinus and indicated that gene flow through the Eastern Pacific Barrier was mostly eastwards, whereas it was westwards between the central and western Pacific. Genetic exchange was high and symmetrical between the western Pacific and the Indian Ocean. Thus, despite the remarkably low morphological variation of Heteropriacanthus, its phylogeography shows that gene flow is restricted by some of the major barriers to dispersal for marine organisms. Nevertheless, the observed degree of connectivity across the width of the Indo-Pacific is remarkable for a reef fish.