The Genomic Signature of Allopatric Speciation in a Songbird Is Shaped by Genome Architecture (Aves: Certhia americana)

The genomic signature of speciation with gene flow is often attributed to the strength of divergent selection and recombination rate in regions harboring targets for selection. In contrast, allopatric speciation provides a different geographic context and evolutionary scenario, whereby introgression is limited by isolation rather than selection against gene flow. Lacking shared divergent selection or selection against hybridization, we would predict the genomic signature of allopatric speciation would largely be shaped by genomic architecture—the nonrandom distribution of functional elements and chromosomal characteristics—through its role in affecting the processes of selection and drift. Here, we built and annotated a chromosome-scale genome assembly for a songbird (Passeriformes: Certhia americana). We show that the genomic signature of allopatric speciation between its two primary lineages is largely shaped by genomic architecture. Regionally, gene density and recombination rate variation explain a large proportion of variance in genomic diversity, differentiation, and divergence. We identified a heterogeneous landscape of selection and neutrality, with a large portion of the genome under the effects of indirect selection. We found higher proportions of small chromosomes under the effects of indirect selection, likely because they have relatively higher gene density. At the chromosome scale, differential genomic architecture of macro- and microchromosomes shapes the genomic signatures of speciation: chromosome size has: 1) a positive relationship with genetic differentiation, genetic divergence, rate of lineage sorting in the contact zone, and proportion neutral evolution and 2) a negative relationship with genetic diversity and recombination rate.