Abstract

Geographically limited dispersal can shape genetic population structure and result in a correlation between genetic and geographic distance, commonly called isolation-by-distance. Despite the prevalence of isolation-by-distance in nature, to date few studies have empirically demonstrated the processes that generate this pattern, largely because few populations have direct measures of individual dispersal and pedigree information. Intensive, long-term demographic studies and exhaustive genomic surveys in the Florida Scrub-Jay (Aphelocoma coerulescens) provide an excellent opportunity to investigate the influence of dispersal on genetic structure. Here, we used a panel of genome-wide SNPs and extensive pedigree information to explore the role of limited dispersal in shaping patterns of isolation-by-distance in both sexes, and at an exceedingly fine spatial scale (within ~10 km). Isolation-by-distance patterns were stronger in male-male and male-female comparisons than in female-female comparisons, consistent with observed differences in dispersal propensity between the sexes. Using the pedigree, we demonstrated how various genealogical relationships contribute to fine-scale isolation-by-distance. Simulations using field-observed distributions of male and female natal dispersal distances showed good agreement with the distribution of geographic distances between breeding individuals of different pedigree relationship classes. Furthermore, we built coalescent simulations parameterized by the observed dispersal curve, population density, and immigration rate, and showed how incorporating these extensions to Malécot’s theory of isolation-by-distance allows us to accurately reconstruct observed sex-specific isolation-by-distance patterns in autosomal and Z-linked SNPs. Therefore, patterns of fine-scale isolation-by-distance in the Florida Scrub-Jay can be well understood as a result of limited dispersal over contemporary timescales.

Highlights

  • The movement of individuals over the landscape influences biological processes and diversity at many levels [1], ranging from interactions between individuals to the persistence of populations or species over time [2,3,4]

  • Geographically-limited dispersal can result in isolation-by-distance, a pattern of increased genetic differentiation [5, 6] or, decreased genetic relatedness [7,8,9] between individuals as geographic distance increases

  • This pattern results because genetic drift can act to differentiate allele frequencies faster than dispersal can homogenize them among geographically distant populations

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Summary

Author summary

Dispersal is a fundamental component of the life history of most organisms and influences many biological processes. We often observe a pattern of decreased genetic relatedness between individuals as geographic distances increases, or isolation-by-distance. This pattern is pronounced in organisms with extremely short dispersal distances. Despite the ubiquity of isolation-by-distance patterns in nature, there are few examples that explicitly demonstrate how limited dispersal influences spatial genetic structure. We investigate the processes that result in spatial genetic structure using the Florida Scrub-Jay, a bird with extremely limited dispersal behavior and extensive genome-wide data. We show how limited dispersal results in close genealogical relatives living closer together geographically, which generates a strong pattern of isolation-by-distance at an extremely small spatial scale (

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