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

Abstract

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.

Complex population structure of the Atlantic puffin revealed by whole genome analyses

“…Such potential geographical separation during the winter season might limit the likelihood of immatures intermixing between the Isle of May and other colonies. Similarly, distinct overwintering distributions have been found to lead to increased genetic diversification in other philopatric seabird species 14,40,43 , such as the thick-billed murre (Uria lomvia) 20 and black-browed albatross (Thalassarche melanophris) 44 . The presence of a Canadian cluster can also be largely explained by their winter distribution around Newfoundland 42,45 .…”

“…The mitogenomic variation suggests that puffins experienced a recent population expansion, possibly out of a refugium after the Last Glacial Maximum. Indeed, it has been shown that mitogenomic variation in seabirds is dominated by historical factors rather than representing contemporary gene flow 40 , and a lack of mitogenomic population structure has been observed in many marine birds with high philopatry e.g. 46,53,54 .…”

“…46,53,54 . In contrast to the mitogenomes, the structure in the nuclear data therefore likely originated after the last glacial period and reflects the influence of relatively recent barriers to gene flow in a context of historical demography 14,40 . Such results are relevant for understanding the "seabird paradox", which contrasts the life-history traits of high philopatry and restricted dispersal in otherwise highly mobile species 55 .…”

Cryptic differentiation in the Manx shearwater hinders the identification of a new endemic subspecies

“…Mechanisms of speciation in seabirds are poorly understood (Friesen 2015). Recently, long-term barriers and population persistence have been proposed as mechanisms for genetic structuring and speciation (Lombal et al 2020), although the high philopatry of seabirds alone could lead to reproductive isolation (Friesen 2015). In addition, allochrony, i.e.…”

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

“…Migration can be variously defined, but is often understood as predictable seasonal movement of individuals between locations, and it is widely but heterogeneously distributed across animals (Dingle and Drake 2007). Although migration does not necessitate spatial shifts in reproduction (i.e., dispersal), a positive association is assumed (Lombal et al 2020). As with other dispersal-related traits, migration presents an interesting conundrum with respect to predicting its impact on diversification (McDowall, 1988(McDowall, , 2001Winker 2000;Corush 2019).…”