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Eco‐phylogeographic approaches to comparative population genetic analyses allow for the inclusion of intrinsic influences as drivers of intraspecific genetic structure. This insight into microevolutionary processes, including changes within a species or lineage, provides better mechanistic understanding of species‐specific interactions and enables predictions of evolutionary responses to environmental change. In this study, we used single nucleotide polymorphisms (SNPs) identified from reduced representation sequencing to compare neutral population structure, isolation by distance (IBD), genetic diversity and effective population size (N_e) across three closely related and co‐distributed saltmarsh sparrow species differing along a specialization gradient—Nelson's (Ammospiza nelsoni subvirgata), saltmarsh (A. caudacuta) and seaside sparrows (A. maritima maritima). Using an eco‐phylogeographic lens within a conservation management context, we tested predictions about species' degree of evolutionary history and ecological specialization to tidal marshes, habitat, current distribution and population status on population genetic metrics. Population structure differed among the species consistent with their current distribution and habitat factors, rather than degree of ecological specialization: seaside sparrows were panmictic, saltmarsh sparrows showed hierarchical structure and Nelson's sparrows were differentiated into multiple, genetically distinct populations. Neutral population genetic theory and demographic/evolutionary history predicted patterns of genetic diversity andN_erather than degree of ecological specialization. Patterns of population variation and evolutionary distinctiveness (Shapely metric) suggest different conservation measures for long‐term persistence and evolutionary potential in each species. Our findings contribute to a broader understanding of the complex factors influencing genetic variation, beyond specialist‐generalist status and support the role of an eco‐phylogeographic approach in population and conservation genetics.

 

Abstract Background Exploring hybrid zone dynamics at different spatial scales allows for better understanding of local factors that influence hybrid zone structure. In this study, we tested hypotheses about drivers of introgression at two spatial scales within the Saltmarsh Sparrow ( Ammospiza caudacuta ) and Nelson’s Sparrow ( A. nelsoni ) hybrid zone. Specifically, we evaluated the influence of neutral demographic processes (relative species abundance), natural selection (exogenous environmental factors and genetic incompatibilities), and sexual selection (assortative mating) in this mosaic hybrid zone. By intensively sampling adults (n = 218) and chicks (n = 326) at two geographically proximate locations in the center of the hybrid zone, we determined patterns of introgression on a fine scale across sites of differing habitat. We made broadscale comparisons of patterns from the center with those of prior studies in the southern edge of the hybrid zone. Results A panel of fixed SNPs (135) identified from ddRAD sequencing was used to calculate a hybrid index and determine genotypic composition/admixture level of the populations. Another panel of polymorphic SNPs (589) was used to assign paternity and reconstruct mating pairs to test for sexual selection. On a broad-scale, patterns of introgression were not explained by random mating within marshes. We found high rates of back-crossing and similarly low rates of recent-generation (F1/F2) hybrids in the center and south of the zone. Offspring genotypic proportions did not meet those expected from random mating within the parental genotypic distribution. Additionally, we observed half as many F1/F2 hybrid female adults than nestlings, while respective male groups showed no difference, in support of Haldane’s Rule. The observed proportion of interspecific mating was lower than expected when accounting for mate availability, indicating assortative mating was limiting widespread hybridization. On a fine spatial scale, we found variation in the relative influence of neutral and selective forces between inland and coastal habitats, with the smaller, inland marsh influenced primarily by neutral demographic processes, and the expansive, coastal marsh experiencing higher selective pressures in the form of natural (exogenous and endogenous) and sexual selection. Conclusions Multiple drivers of introgression, including neutral and selective pressures (exogenous, endogenous, and sexual selection), are structuring this hybrid zone, and their relative influence is site and context-dependent.