Genomic variation across two barn swallow hybrid zones reveals traits associated with divergence in sympatry and allopatry

Abstract

Hybrid zones are geographic regions where isolating barriers between divergent populations are challenged by admixture. Identifying factors that facilitate or inhibit hybridization in sympatry can illuminate the processes that maintain those reproductive barriers. We analysed patterns of hybridization and phenotypic variation across two newly discovered hybrid zones between three subspecies of barn swallow (Hirundo rustica). These subspecies differ in ventral coloration and wing length, traits that are targets of sexual and natural selection, respectively, and are associated with genome-wide differentiation in allopatry. We tested the hypothesis that the degree of divergence in these traits is associated with the extent of hybridization in secondary contact. We applied measures of population structure based on >23,000 SNPs to confirm that named subspecies correspond to distinct genomic clusters, and assessed coincidence between geographic clines for ancestry and phenotype. Although gene flow was ongoing across both hybrid zones and pairwise F between subspecies was extremely low, we found striking differences in the extent of hybridization. In the more phenotypically differentiated subspecies pair, clines for ancestry, wing length and ventral coloration were steep and coincident, suggestive of strong isolation and, potentially, selection associated with phenotype. In the less phenotypically differentiated pair, gene flow and phenotypic variation occurred over a wide geographic span, indicative of weaker isolation. Traits associated with genome-wide differentiation in allopatry may thus also contribute to isolation in sympatry. We discuss potentially important additional roles for evolutionary history and ecology in shaping variation in the extent hybridization between closely related pairs of subspecies.

Cryptic and extensive hybridization between ancient lineages of American crows

“…We compared genomic hybrid indices to intertaxon heterozygosities to determine whether individual crows were recent‐generation hybrids or descendants of long‐admixed populations (Bouchemousse et al, 2016; Milne & Abbott, 2008). We designated crows as parental American or parental Northwestern if these respective ancestry proportions exceeded 0.98 in our combined K = 2 Bayesian clustering runs (Scordato et al, 2017). We used a custom R script to subset the 62‐sample SNP alignment containing missing data to include only parental individuals and only variable, unlinked SNPs present for ≥ 75% of individuals.…”

“…With this alignment we calculated genome‐wide and SNP‐specific F ST between parental populations with r package Hierfstat (Goudet, 2005). We considered SNPs with F ST > 0.6 to be ancestry‐informative (Scordato et al, 2017) and further limited our alignment to these SNPs using a custom r script. For each individual crow, we calculated a maximum likelihood estimate of the genomic hybrid index and the average intertaxon heterozygosity across ancestry‐informative loci using r package Introgress (Gompert & Buerkle, 2010).…”

“…Heterozygosity is reduced in later‐generation hybrids and backcrosses. We considered crows with hybrid index > 0.25 and < 0.75 and heterozygosity > 0.5 to be recent‐generation hybrids, individuals with hybrid index > 0.25 and < 0.75 but with heterozygosity < 0.5 to be later‐generation hybrids, and birds with hybrid index < 0.25 or > 0.75 to be backcrosses (Larson, White, Ross, & Harrison, 2014; Milne & Abbott, 2008; Scordato et al, 2017; Toews, Lovette, Irwin, & Brelsford, 2018).…”

“…For mtDNA, we fit a cline model for population frequencies of American mtDNA (range 0–1) using hzar.doMolecularData1DPops and hzar.makeCline1DFreq. For overall nuDNA, we fit a cline model to means and variances of population ancestry proportions ( q values) from combined K = 2 Bayesian clustering runs using hzar.doNormalData1DPops and hzar.makeCline1DNormal (Leaché et al, 2017; Linck et al, 2019; Scordato et al, 2017). For both mtDNA and overall nuDNA, we fit models without exponential tails, restricted parameter search space to a liberal yet reasonable range of values (cline centre > 500 km and < 3,500 km, cline width < 3,500 km; Derryberry et al, 2014) and fixed means, variances, and allele frequencies at cline ends to the observed values of the terminal populations (Linck et al, 2019; Lipshutz et al, 2019).…”

“…Examples include identifying geographic clusters of genetically homogenous individuals, identifying independent evolutionary lineages, establishing phylogenetic relatedness of lineages, and estimating divergence dates (Struck et al, 2018). In geographic areas where genetically differentiated individuals co‐occur, the presence or absence of genomic admixture indicates either hybridization or reproductive isolation (e.g., Linck et al, 2019; Pulido‐Santacruz, Aleixo, & Weir, 2018; Scordato et al, 2017).…”