Assortative mate choice and epistatic mating-trait architecture induce complex movement of the crow hybrid zone

Abstract

Hybrid zones provide a window into the evolutionary processes governing species divergence. While the role of postzygotic isolation has been extensively characterized, the contribution of prezygotic isolation is less well explored. In particular, the effect of mate choice mediated by preference learning such as self-recognition or imprinting remains largely elusive. Here, we present model-based simulations investigating the influence of the preference function, the genetic architecture of the mating trait and the role of sexual selection on spatio-temporal hybrid zone dynamics. The model is parameterized with empirical data from the hybrid zone between all-black carrion and grey-coated hooded crows allowing qualitative and quantitative inference in a natural setting. The best-fit model resulted in narrow clines for the mating trait loci coding for color polymorphism maintained by a moderate degree of assortative mating. Epistasis induced hybrid zone movement in favor of dark alleles followed by a shift in the opposite direction ∼1,200 generations after secondary contact. Unlinked neutral loci diffused near-unimpeded across the zone. This study demonstrates that assortative mating can explain steep transitions in mating trait loci without generalizing to genome-wide reproductive isolation. It further emphasizes the importance of mating trait architecture for spatiotemporal hybrid zone dynamics.

Asymmetric introgression reveals the genetic architecture of a plumage trait

“…that assortative mating coupled with this epistatic genetic architecture can alone promote sexual trait introgression similar to results presented here 19 . Together, these results and our own findings support the long-standing hypothesis 17 , that peculiarities of barrier trait architecture governed by dominance, epistasis, or both, can drive asymmetric introgression.…”

“…Asymmetric sexual or natural selection is often invoked to explain this pattern. Indeed, simulation studies suggest that differences in allele fitness and selection strength 17,18 , as well as epistasis 19 , and deviation from codominant genetic inheritance of selected phenotypes 17 can contribute to asymmetric introgression. However, there exist few empirical examples in the literature due to the difficulty of dissecting the genetic architecture of phenotypic traits in natural study systems-data crucial for distinguishing among these potential mechanisms.…”

“…However, there exist few empirical examples in the literature due to the difficulty of dissecting the genetic architecture of phenotypic traits in natural study systems-data crucial for distinguishing among these potential mechanisms. Furthermore, the connection between trait genetic architecture and asymmetric introgression under a scenario of positive assortative matingcommonly found in the hybrid zones-remains poorly understood 19 .…”

Discovery and population genomics of structural variation in a songbird genus

“…Taken together, these results render this LTR retrotransposon insertion a prime candidate mutation underlying plumage divergence in hooded and carrion crows, and add to the notion that transposable elements are important contributors to the genetic architecture of phenotypic change 3,43 . Given the importance of color variation to prezygotic isolation in this system 21,25,49 it constitutes an example of a structural mutation with evolutionary significance. Since the majority of SV is likely still uncovered in most organisms 50 , these results represent an important hallmark for the field, highlighting the need for rigorous methodological approaches and the evolutionary importance of SV in natural populations.…”

“…The genetic basis of plumage variation and its contribution to population divergence has been investigated in much detail using single-nucleotide polymorphism (SNP) data in the Corvus (corone) spp. species complex that is characterized by narrow contact zones between all-black forms (C. (c.) corone/ orientalis) and populations consisting of the pied phenotype (C. (c.) cornix/capellanus/pallescens/pectoralis/sharpii) [20][21][22] . These studies suggest that phenotypically well differentiated populations diverged during the late Pleistocene and exhibit low levels of genome-wide differentiation 23 .…”