Genome-Wide Dissection of Hybrid Sterility in Drosophila Confirms a Polygenic Threshold Architecture

Abstract

To date, different studies about the genetic basis of hybrid male sterility (HMS), a postzygotic reproductive barrier thoroughly investigated using Drosophila species, have demonstrated that no single major gene can produce hybrid sterility without the cooperation of several genetic factors. Early work using hybrids between Drosophila koepferae (Dk) and Drosophila buzzatii (Db) was consistent with the idea that HMS requires the cooperation of several genetic factors, supporting a polygenic threshold (PT) model. Here we present a genome-wide mapping strategy to test the PT model, analyzing serially backcrossed fertile and sterile males in which the Dk genome was introgressed into the Db background. We identified 32 Dk-specific markers significantly associated with hybrid sterility. Our results demonstrate 1) a strong correlation between the number of segregated sterility markers and males' degree of sterility, 2) the exchangeability among markers, 3) their tendency to cluster into low-recombining chromosomal regions, and 4) the requirement for a minimum number (threshold) of markers to elicit sterility. Although our findings do not contradict a role for occasional major hybrid-sterility genes, they conform more to the view that HMS primarily evolves by the cumulative action of many interacting genes of minor effect in a complex PT architecture.

Coadapted genomes and selection on hybrids: Fisher's geometric model explains a variety of empirical patterns

“…Data—including those analyzed here—suggest that such architectures might be quite common (Davis and Wu 1996; Maside and Naveira 1996; Rosas et al. 2010; Morán and Fontdevila 2014; Baird 2017; Buerkle 2017; Boyle et al. 2017).…”

Interspecific hybridization as a genomic stressor inducing mobilization of transposable elements inDrosophila

“…koepfere hybrids and raises de question about the involvement of TE mobilization in hybrid sterility and the molecular causes. Previous genetic work, with these same hybrids, proposes that male hybrid sterility results from the cumulative action of many interacting genes of minor effects 26 . We ignore the direct impact of TE derepression in fecundity of D. buzzatii/D.…”

Coadapted genomes and selection on hybrids: Fisher’s geometric model explains a variety of empirical patterns

“…Given its ability to interpolate between models of different and extreme kinds, it should also be particularly useful for understanding hybridization in intermediate regimes,486 where parental genomes are characterized by both maladaptation and allelic coadaptation, or where the architecture of isolation involves many genes of small or moderate effect. Data -including those 488 analyzed here -suggest that such architectures might be quite common(Baird 2017;Boyle et al 2017;Buerkle 2017;Davis and Wu 1996;Maside and Naveira 1996;Morán and Fontdevila 2014).…”

“…Duranton et al 2017; Fraïsse et al 2016a,b; Mendez et al 2012), the effects of recombination in shaping 470 patterns of divergence(Schumer et al 2017), and the roles of intrinsic versus extrinsic isolation(Chevin et al 2014). Given its ability to interpolate between models of different and extreme kinds, it should 472 also be particularly useful for understanding hybridization in intermediate regimes, where parental genomes are characterized by both maladaptation and allelic coadaptation, or where the architecture of 474 isolation involves many genes of small or moderate effect(Baird 2017;Boyle et al 2017;Buerkle 2017;Davis and Wu 1996; Maside and Naveira 1996;Morán and Fontdevila 2014).…”