Identifying mechanisms of genetic differentiation among populations in vagile species: historical factors dominate genetic differentiation in seabirds

Elucidating the factors underlying the origin and maintenance of genetic variation among populations is crucial for our understanding of their ecology and evolution, and also to help identify conservation priorities. While intrinsic movement has been hypothesized as the major determinant of population genetic structuring in abundant vagile species, growing evidence indicates that vagility does not always predict genetic differentiation. However, identifying the determinants of genetic structuring can be challenging, and these are largely unknown for most vagile species. Although, in principle, levels of gene flow can be inferred from neutral allele frequency divergence among populations, underlying assumptions may be unrealistic. Moreover, molecular studies have suggested that contemporary gene flow has often not overridden historical influences on population genetic structure, which indicates potential inadequacies of any interpretations that fail to consider the influence of history in shaping that structure. This exhaustive review of the theoretical and empirical literature investigates the determinants of population genetic differentiation using seabirds as a model system for vagile taxa. Seabirds provide a tractable group within which to identify the determinants of genetic differentiation, given their widespread distribution in marine habitats and an abundance of ecological and genetic studies conducted on this group. Herein we evaluate mitochondrial DNA (mtDNA) variation in 73 seabird species. Lack of mutation–drift equilibrium observed in 19% of species coincided with lower estimates of genetic differentiation, suggesting that dynamic demographic histories can often lead to erroneous interpretations of contemporary gene flow, even in vagile species. Presence of land across the species sampling range, or sampling of breeding colonies representing ice‐free Pleistocene refuge zones, appear to be associated with genetic differentiation in Tropical and Southern Temperate species, respectively, indicating that long‐term barriers and persistence of populations are important for their genetic structuring. Conversely, biotic factors commonly considered to influence population genetic structure, such as spatial segregation during foraging, were inconsistently associated with population genetic differentiation. In light of these results, we recommend that genetic studies should consider potential historical events when identifying determinants of genetic differentiation among populations to avoid overestimating the role of contemporary factors, even for highly vagile taxa.     

Does migration promote or inhibit diversification? A case study involving the dominant radiation of temperate Southern Hemisphere freshwater fishes

Although theory predicts that dispersal has a pivotal influence on speciation and extinction rates, it can have contradictory effects on each, such that empirical quantification of its role is required. In many studies, dispersal reduction appears to promote diversification, although some comparisons of migratory and nonmigratory species suggest otherwise. We tested for a relationship between migratory status and diversification rate within the dominant radiation of temperate Southern Hemisphere freshwater fishes, the Galaxiidae. We reconstructed a molecular phylogeny comprising >95% of extant taxa, and applied State-dependent Speciation Extinction models to estimate speciation, extinction, and diversification rates. In contrast to some previous studies, we revealed higher diversification rates in nonmigratory lineages. The reduced gene flow experienced by nonmigratory galaxiids appears to have increased diversification under conditions of allopatry or local adaptation. Migratory galaxiid lineages, by contrast, are genetically homogeneous within landmasses, but may also be rarely able to diversify by colonizing other landmasses in the temperate Southern Hemisphere. Apparent contradictions among studies of dispersal-diversification relationships may be explained by the spatial context of study systems relative to species dispersal abilities, by means of the “intermediate dispersal” model; the accurate quantification of dispersal abilities will aid in the understanding of these proposed interactions.