Bidirectional adaptive introgression between two ecologically divergent sparrow species

Abstract

Natural hybrid zones can be used to dissect the mechanisms driving key evolutionary processes by allowing us to identify genomic regions important for establishing reproductive isolation and that allow for transfer of adaptive variation. We leverage whole-genome data in a system where two bird species, the saltmarsh (Ammospiza caudacuta) and Nelson's (A. nelsoni) sparrow, hybridize despite their relatively high background genetic differentiation and past ecological divergence. Adaptive introgression is plausible in this system because Nelson's sparrows are recent colonists of saltwater marshes, compared to the specialized saltmarsh sparrow that has a longer history of saltmarsh adaptation. Comparisons among whole-genome sequences of 34 individuals from allopatric and sympatric populations show that ongoing gene flow is shaping the genomic landscape, with allopatric populations exhibiting genome-wide F estimates close to double of that observed in sympatry. We characterized patterns of introgression across the genome and identify regions that exhibit biased introgression into hybrids from one parental species. These regions offer compelling candidates for genes related to tidal marsh adaptations suggesting that adaptive introgression may be an important consequence of hybridization. These findings highlight the value of considering the landscapes of both genome-wide introgression and divergence when characterizing the evolutionary forces that drive speciation.

Ancestral hybridisation facilitated species diversification in the Lake Malawi cichlid fish adaptive radiation

“…A clear message from the increasing number of genomic investigations of non-model organisms is that hybridisation between related species is far more common than previously thought, leading to fundamentally reticulate patterns of evolution, where species relationships are represented by networks rather than trees. In many cases it has been shown that this process can transport selectively favourable alleles between species and thus contribute to adaptation (Herman et al 2018;Suarez-Gonzalez et al 2018;Walsh et al 2018;Moest et al 2019) . However, the effect of such hybridisation events on biological diversification, that is, whether it increases or reduces the rate at which new species emerge over time is not generally understood.…”

Divergent selection and drift shape the genomes of two avian sister species spanning a saline–freshwater ecotone

“…Divergence via drift in allopatry therefore may have progressed unfettered from potential homogenizing effects of gene flow, resulting in the observed patterns of high divergence across the genomic landscape (sensu Feder, Egan, & Nosil, ). Support for this idea comes from a study comparing whole genomes of saltmarsh and Nelson's sparrows from allopatric and sympatric populations (Walsh, Kovach, Olsen, Shriver, & Lovette, ). That study found that only about 5% of the fixed differences found in allopatry are present in sympatric populations, suggesting that when populations co‐occur contemporary gene flow homogenizes all but a small portion of the genomic landscape, which likely comprises important barrier loci (loci important in reproductive isolation; Feder et al, ; Nosil & Feder, ).…”

Differential introgression of a female competitive trait in a hybrid zone between sex‐role reversed species

“…; Bay and Ruegg ; Walsh et al. ). Traits involved in mate choice are typically thought to promote reproductive isolation, and are thus expected to have restricted introgression compared with ecological traits (Bridle et al.…”

“…This introgression can be asymmetric, whereby traits and their associated genes transition from one population into another more extensively than in the other direction. Many examples of introgression are based on traits involved in local adaptation (Pardo-Diaz et al 2012;Racimo et al 2015;Lamichhaney et al 2015;Bay and Ruegg 2017;Walsh et al 2018). Traits involved in mate choice are typically thought to promote reproductive isolation, and are thus expected to have restricted introgression compared with ecological traits (Bridle et al 2002).…”