Estimating dispersal from genetic isolation by distance in a coral reef fish (Hypoplectrus puella).

The spatial scale of dispersal in coral reef fishes eludes ecologists despite the importance of this parameter for understanding the dynamics of ecological and evolutionary processes. Genetic isolation by distance (IBD) has been used to estimate dispersal in coral reef fishes, but its application in marine systems has been limited by insufficient sampling at different spatial scales and a lack of information regarding population density. Here, we present an analysis of IBD in the barred hamlet (Hypoplectrus puella, Serranidae) at spatial scales ranging from 10 to 3200 km complemented with SCUBA surveys of population densities covering 94000 m2 of reef. We used 10 hypervariable DNA markers to genotype 854 fish from 15 locations, and our results establish that IBD in H. puella emerges at a spatial scale of 175 km and is preserved up to the regional scale (3200 km). Assuming a normal or a Laplace dispersal function, our data are consistent with mean dispersal distances in H. puella that range between 2 and 14 km. Such small mean dispersal distances is a surprising result given the three-week pelagic larval duration of H. puella and the low level of genetic structure at the Caribbean scale (Wright's fixation index, F(ST), estimate = 0.005). Our data reinforce the importance of considering population density when estimating dispersal from IBD and underscore the relevance of sampling at local scales, even when genetic structure is weak at the regional scale.

Population genetic analyses of Hypoplectrus coral reef fishes provide evidence that local processes are operating during the early stages of marine adaptive radiations.

Large-scale, spatially explicit models of adaptive radiation suggest that the spatial genetic structure within a species sampled early in the evolutionary history of an adaptive radiation might be higher than the genetic differentiation between different species formed during the same radiation over all locations. Here we test this hypothesis with a spatial population genetic analysis of Hypoplectrus coral reef fishes (Serranidae), one of the few potential cases of a recent adaptive radiation documented in the marine realm. Microsatellite analyses of Hypoplectrus puella (barred hamlet) and Hypoplectrus nigricans (black hamlet) from Belize, Panama and Barbados validate the population genetic predictions at the regional scale for H. nigricans despite the potential for high levels of gene flow between populations resulting from the 3-week planktonic larval phase of Hypoplectrus. The results are different for H. puella, which is characterized by significantly lower levels of spatial genetic structure than H. nigricans. An extensive field survey of Hypoplectrus population densities complemented by individual-based simulations shows that the higher abundance and more continuous distribution of H. puella could account for the reduced spatial genetic structure within this species. The genetic and demographic data are also consistent with the hypothesis that H. puella might represent the ancestral form of the Hypoplectrus radiation, and that H. nigricans might have evolved repeatedly from H. puella through ecological speciation. Altogether, spatial genetic analysis within and between Hypoplectrus species indicate that local processes can operate at a regional scale within recent marine adaptive radiations.

Colour pattern as a single trait driving speciation in Hypoplectrus coral reef fishes?

Theory shows that speciation in the presence of gene flow occurs only under narrow conditions. One of the most favourable scenarios for speciation with gene flow is established when a single trait is both under disruptive natural selection and used to cue assortative mating. Here, we demonstrate the potential for a single trait, colour pattern, to drive incipient speciation in the genus Hypoplectrus (Serranidae), coral reef fishes known for their striking colour polymorphism. We provide data demonstrating that sympatric Hypoplectrus colour morphs mate assortatively and are genetically distinct. Furthermore, we identify ecological conditions conducive to disruptive selection on colour pattern by presenting behavioural evidence of aggressive mimicry, whereby predatory Hypoplectrus colour morphs mimic the colour patterns of non-predatory reef fish species to increase their success approaching and attacking prey. We propose that colour-based assortative mating, combined with disruptive selection on colour pattern, is driving speciation in Hypoplectrus coral reef fishes.