Hybrid Sterility, Genetic Conflict and Complex Speciation: Lessons From the Drosophila simulans Clade Species

Abstract

The three fruitfly species of the Drosophila simulans clade— D. simulans, D. mauritiana, and D. sechellia— have served as important models in speciation genetics for over 40 years. These species are reproductively isolated by geography, ecology, sexual signals, postmating-prezygotic interactions, and postzygotic genetic incompatibilities. All pairwise crosses between these species conform to Haldane’s rule, producing fertile F1 hybrid females and sterile F1 hybrid males. The close phylogenetic proximity of the D. simulans clade species to the model organism, D. melanogaster, has empowered genetic analyses of their species differences, including reproductive incompatibilities. But perhaps no phenotype has been subject to more continuous and intensive genetic scrutiny than hybrid male sterility. Here we review the history, progress, and current state of our understanding of hybrid male sterility among the D. simulans clade species. Our aim is to integrate the available information from experimental and population genetics analyses bearing on the causes and consequences of hybrid male sterility. We highlight numerous conclusions that have emerged as well as issues that remain unresolved. We focus on the special role of sex chromosomes, the fine-scale genetic architecture of hybrid male sterility, and the history of gene flow between species. The biggest surprises to emerge from this work are that (i) genetic conflicts may be an important general force in the evolution of hybrid incompatibility, (ii) hybrid male sterility is polygenic with contributions of complex epistasis, and (iii) speciation, even among these geographically allopatric taxa, has involved the interplay of gene flow, negative selection, and positive selection. These three conclusions are marked departures from the classical views of speciation that emerged from the modern evolutionary synthesis.

Hybrid fitness effects modify fixation probabilities of introgressed alleles

“…We describe the evolutionary dynamics of a semidominant introgressed B allele, which depend on locus-specific fitness effects as well as HFEs. We assume that heterosis and DMI effects are polygenic as per empirical results from True et al (1996) and Presgraves and Meiklejohn (2021) , implying that each additional unlinked effect makes an infinitesimal contribution to the overall strength of HFEs. Due to repeated backcrossing within the recipient population, introgressed donor DNA is diluted each generation.…”

“…As we show in the Supplementary Materials , the multiplicative model is approximated by an additive model if the effect of each DMI is small. This is a valid assumption given the polygenic nature of DMI effects ( True et al 1996 ; Presgraves and Meiklejohn 2021 ).…”

“…This hybrid breakdown can be induced by introgression introducing segregated variants into a new genomic context, which may cause so-called Dobzhansky-Muller incompatibilities (DMIs) ( Kondrashov et al 2002 ). DMIs arise from untested epistatic interactions of two or more alleles ( Dobzhansky 1937 ; Muller 1942 ; Fraïsse et al 2014 ; Presgraves and Meiklejohn 2021 ), i.e. interactions between alleles from different source populations.…”

Influence of Gender Bias on Distribution of Hybrid Sterility in Rice

“…Thus, f TRD and siTRD offers a selective disadvantage on the individual. The abundance of male sterility in hybrids is also found in Drosophila (Presgraves and Meiklejohn, 2021). A much smaller selective disadvantage of male sterility genes might help them exist within diverse populations at a higher pace of frequency.…”

The contribution of sex chromosome conflict to disrupted spermatogenesis in hybrid house mice

“…Sex chromosomes are often involved in the evolution of hybrid male sterility between animal species (Coyne and Orr 1989; Turelli and Orr 2000; Presgraves and Meiklejohn 2021). Referred to as the large X-effect in X-Y systems (Coyne and Orr 1989), it remains unclear to what extent this general pattern reflects common evolutionary processes or functional mechanisms unique to sex chromosomes (Meiklejohn and Tao 2010).…”