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.
Highlights
From Darwin’s Origin of Species, to the modern evolutionary synthesis (Dobzhansky, 1937), and into the present era (Coyne and Orr, 2004), hybrid incompatibility— the intrinsic sterility or inviability of species hybrids— has held a central place in speciation research
The D. simulans clade species have been at the forefront of modern speciation genetics for over 40 years
We have learned that HMS in the D. simulans clade accumulates faster on the X chromosome
Summary
From Darwin’s Origin of Species, to the modern evolutionary synthesis (Dobzhansky, 1937), and into the present era (Coyne and Orr, 2004), hybrid incompatibility— the intrinsic sterility or inviability of species hybrids— has held a central place in speciation research. A major limitation of these species for genetic analysis of reproductive incompatibilities, is their age: as D. melanogaster diverged from D. simulans ∼3 Mya, all of their hybrids are dead or sterile, and genetic analyses involving D. melanogaster are limited, under most circumstances, to F1 hybrids [but see Sawamura et al (2000); Masly et al (2006))]. This problem has been circumvented in part by the discovery of “hybrid rescue mutations”— compatible alleles at otherwise incompatible loci that completely (or nearly so) reverse hybrid lethality (Watanabe, 1979; Hutter and Ashburner, 1987). Rather than present a taxonomically comprehensive review, we focus narrowly on lessons from the D. simulans clade species
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