Hybrid speciation through sorting of parental incompatibilities in Italian sparrows

Abstract

Speciation by hybridization is emerging as a significant contributor to biological diversification. Yet, little is known about the relative contributions of (i) evolutionary novelty and (ii) sorting of pre-existing parental incompatibilities to the build-up of reproductive isolation under this mode of speciation. Few studies have addressed empirically whether hybrid animal taxa are intrinsically isolated from their parents, and no study has so far investigated by which of the two aforementioned routes intrinsic barriers evolve. Here, we show that sorting of pre-existing parental incompatibilities contributes to intrinsic isolation of a hybrid animal taxon. Using a genomic cline framework, we demonstrate that the sex-linked and mitonuclear incompatibilities isolating the homoploid hybrid Italian sparrow at its two geographically separated hybrid-parent boundaries represent a subset of those contributing to reproductive isolation between its parent species, house and Spanish sparrows. Should such a sorting mechanism prove to be pervasive, the circumstances promoting homoploid hybrid speciation may be broader than currently thought, and indeed, there may be many cryptic hybrid taxa separated from their parent species by sorted, inherited incompatibilities.

Rapid acceleration of plant speciation during the Anthropocene

“…In addition, new species are coming into existence at the same time as the extinctions, rather than their origins being delayed by millions of years. Hybrid speciation is substantially more frequent in plants than in animals, although some anthropogenic hybrid animal species have arisen recently [14,42,43], and behaviourally mediated sympatric speciation rates in novel humancreated environments may be higher for animals than for plants [17]. I suggest that animal speciation is also accelerating, but not as rapidly as in plants.…”

The genomic mosaicism of hybrid speciation

“…Evidence for postzygotic reproductive barriers has been shown in areas of contact ( 13 ). Furthermore, hybridization is likely to have directly contributed to the development of reproductive barriers between the Italian sparrow and its parents as preexisting parental incompatibility alleles are sorted within the Italian sparrow lineage ( 14 ). …”

Reticulation, divergence, and the phylogeography–phylogenetics continuum

“…2). Finally, reticulation is becoming increasingly conspicuous at the level of diverging species and adaptive radiations (25,35,(41)(42)(43)(44), and is causing biologists to consider "ephemeral species," with frequent lineage mergers, not only among sister taxa but between lineages with any geographic co-occurrence (45). The goal, however imperfect it is now realized, is to develop and apply models that integrate phylogeography, demography, and genome evolution in ways that will allow more nuanced interpretation of myriad interacting evolutionary processes from patterns of genomic diversity (46).…”