Could specialization to cold-water upwelling systems influence gene flow and population differentiation in marine organisms? A case study using the blue-footed booby, Sula nebouxii

Abstract

Aim We assessed population differentiation and gene flow across the range of the blue-footed booby (Sula nebouxii) (1) to test the generality of the hypothesis that tropical seabirds exhibit higher levels of population genetic differentiation than their northern temperate counterparts, and (2) to determine if specialization to cold-water upwelling systems increases dispersal, and thus gene flow, in blue-footed boobies compared with other tropical sulids. Location Work was carried out on islands in the eastern tropical Pacific Ocean from Mexico to northern Peru. Methods We collected samples from 173 juvenile blue-footed boobies from nine colonies spanning their breeding distribution and used molecular markers (540 base pairs of the mitochondrial control region and seven microsatellite loci) to estimate population genetic differentiation and gene flow. Our analyses included classic population genetic estimation of pairwise population differentiation, population growth, isolation by distance, associations between haplotypes and geographic locations, and analysis of molecular variance, as well as Bayesian analyses of gene flow and population differentiation. We compared our results with those for other tropical seabirds that are not specialized to cold-water upwellings, including brown (Sula leucogaster), red-footed (S. sula) and masked (S. dactylatra) boobies. Results Blue-footed boobies exhibited weak global population differentiation at both mitochondrial and nuclear loci compared with all other tropical sulids. We found evidence of high levels of gene flow between colonies within Mexico and between colonies within the southern portion of the range, but reduced gene flow between these regions. We also found evidence for population growth, isolation by distance and weak phylogeographic structure. Main conclusions Tropical seabirds can exhibit weak genetic differentiation across large geographic distances, and blue-footed boobies exhibit the weakest population differentiation of any tropical sulid studied thus far. The weak population genetic structure that we detected in blue-footed boobies may be caused by increased dispersal, and subsequently increased gene flow, compared with other sulids. Increased dispersal by blue-footed boobies may be the result of the selective pressures associated with cold-water upwelling systems, to which blue-footed boobies appear specialized. Consideration of foraging environment may be particularly important in future studies of marine biogeography.