Studies that are successful at showing both genomic evidence of divergent selection and a genetic basis to diverging phenotypes at fine spatial scales are generally restricted to traits controlled by few genes of large effect (e.g., Laurent et al., 2016 Linnen et al., 2013 Nosil et al., 2018 Pfeifer et al., 2018). While many studies clearly demonstrate phenotypic and genetic variation consistent with hypotheses of microgeographic adaptive evolution (e.g., Charmantier et al., 2016 Maciejewski et al., 2020 Pequeno et al., 2021), determining the environmental factors and evolutionary and genetic mechanisms driving these patterns remains a difficult challenge (Barrett & Hoekstra, 2011 Hoban et al., 2016). Recent evidence indicates that adaptive divergence driven by strong divergent selection is also possible in highly mobile animals with significant levels of dispersal and gene flow (e.g., Hohenlohe et al., 2010 Mikles et al., 2020 Nacci et al., 2016 Torres‐Dowdall et al., 2012 Urban et al., 2017). Early examples of microgeographic adaptation involved strong divergent selection over very small spatial scales in plants (Antonovics, 2006 Turner et al., 2010). Microgeographic adaptation is a specific case of local adaptation that occurs within the “dispersal neighborhood” of a species, defined as two standard deviations of the dispersal distribution of a population (Richardson et al., 2014 Wright, 1943, 1946). Yet there is mounting evidence that “microgeographic” adaptation in the absence of geographic barriers may be more common than predicted by traditional models (reviewed by Richardson et al., 2014). The homogenizing effects of gene flow on local adaptation (Akerman & Bürger, 2014 Slatkin, 1973, 1987) have led to the dominant paradigm that isolation is generally a prerequisite for adaptive divergence among populations (Garant et al., 2007 Kawecki & Ebert, 2004 Lenormand, 2002 Nosil, 2008 Yeaman & Whitlock, 2011). Much research has focused on the interaction between gene flow and selection in shaping patterns of local adaptation across selective landscapes (Haldane, 1930 Räsänen & Hendry, 2008 Tigano & Friesen, 2016). Understanding the processes that generate and maintain adaptive phenotypic variation is a fundamental goal of evolutionary biology. Our findings support the hypothesis that divergent selection at microgeographic scales can cause adaptive divergence in the presence of ongoing gene flow.
Finally, two genome‐wide association analyses revealed a polygenic basis to variation in bill length with multiple loci detected in or near genes known to affect bill morphology in other birds.
We also found 168 putatively adaptive loci associated with habitat type using multivariate redundancy analysis while controlling for spatial effects. Neutral landscape genomic analyses revealed that genome‐wide genetic differentiation was primarily related to geographic distance and differences in habitat composition. To test whether individuals exhibit genetic differentiation related to habitat type and divergence in bill length, we genotyped over 3000 single nucleotide polymorphisms in 123 adult island scrub‐jay males from across Santa Cruz Island using restriction site‐associated DNA sequencing. The island scrub‐jay ( Aphelocoma insularis) exhibits microgeographic divergence in bill morphology across pine–oak ecotones on Santa Cruz Island, California (USA), similar to adaptive differences described in mainland congeners over much larger geographic scales.
We investigated the potential mechanisms driving habitat‐linked genetic divergence within a bird species endemic to a single 250‐km 2 island.
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