Evolution of Postmating Reproductive Isolation: The Composite Nature of Haldane's Rule and Its Genetic Bases

Davis, A. W.

doi:10.1086/285534

Cited by 354 publications

(83 citation statements)

References 59 publications

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“…For example, sexual conflict can be modeled by assuming that there are differences in the optimal trait values for each sex (Connallon and Clark 2014). Alternatively, we could assume that some subset of the traits is under selection in only one sex, for example traits involved in spermatogenesis or oogenesis (Wu and Davis 1993; Coyne and Orr 2004). Finally, we could assume that sexes are under identical selection, which will usually require assumptions about dosage compensation (see below and Fraïsse et al.…”

Section: Results With Haploid Geneticsmentioning

confidence: 99%

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

2018

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Natural selection plays a variety of roles in hybridization, speciation, and admixture. Most research has focused on two extreme cases: crosses between closely related inbred lines, where hybrids are fitter than their parents, or crosses between effectively isolated species, where hybrids suffer severe breakdown. But many natural populations must fall into intermediate regimes, with multiple types of gene interaction, and these are more difficult to study. Here, we develop a simple fitness landscape model, and show that it naturally interpolates between previous modeling approaches, which were designed for the extreme cases, and invoke either mildly deleterious recessives, or discrete hybrid incompatibilities. Our model yields several new predictions, which we test with genomic data from Mytilus mussels, and published data from plants (Zea, Populus, and Senecio) and animals (Mus, Teleogryllus, and Drosophila). The predictions are generally supported, and the model explains a number of surprising empirical patterns. Our approach enables novel and complementary uses of genome‐wide datasets, which do not depend on identifying outlier loci, or “speciation genes” with anomalous effects. Given its simplicity and flexibility, and its predictive successes with a wide range of data, the approach should be readily extendable to other outstanding questions in the study of hybridization.

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Section: Results With Haploid Geneticsmentioning

confidence: 99%

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

2018

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“…Interestingly, effects on male fertility were seen before any effects were apparent on female viability in all F 1 hybrid birds [83]. In fact, male sterility is at least 10 times more prevalent than inviability in hybrids in general [84] suggesting that male fertility may be especially affected, irrespective of the way sex is determined.…”

Section: Factors That Counteract the Sex-specific Selective Sievementioning

confidence: 95%

The costs of being male: are there sex-specific effects of uniparental mitochondrial inheritance?

Beekman

Dowling

Aanen

2014

Phil. Trans. R. Soc. B

128

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Eukaryotic cells typically contain numerous mitochondria, each with multiple copies of their own genome, the mtDNA. Uniparental transmission of mitochondria, usually via the mother, prevents the mixing of mtDNA from different individuals. While on the one hand, this should resolve the potential for selection for fast-replicating mtDNA variants that reduce organismal fitness, maternal inheritance will, in theory, come with another set of problems that are specifically relevant to males. Maternal inheritance implies that the mitochondrial genome is never transmitted through males, and thus selection can target only the mtDNA sequence when carried by females. A consequence is that mtDNA mutations that confer male-biased phenotypic expression will be prone to evade selection, and accumulate. Here, we review the evidence from the ecological, evolutionary and medical literature for male specificity of mtDNA mutations affecting fertility, health and ageing. While such effects have been discovered experimentally in the laboratory, their relevance to natural populations—including the human population—remains unclear. We suggest that the existence of male expression-biased mtDNA mutations is likely to be a broad phenomenon, but that these mutations remain cryptic owing to the presence of counter-adapted nuclear compensatory modifier mutations, which offset their deleterious effects.

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“…Second, the faster-male theory posits that incompatibilities causing hybrid male sterility accumulate faster than those causing hybrid inviability or hybrid female sterility [8,30]. Two processes might give rise to such faster-male evolution.…”

Section: Introductionmentioning

confidence: 99%

High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila

2007

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Postzygotic reproductive isolation is characterized by two striking empirical patterns. The first is Haldane's rule—the preferential inviability or sterility of species hybrids of the heterogametic (XY) sex. The second is the so-called large X effect—substitution of one species's X chromosome for another's has a disproportionately large effect on hybrid fitness compared to similar substitution of an autosome. Although the first rule has been well-established, the second rule remains controversial. Here, we dissect the genetic causes of these two rules using a genome-wide introgression analysis of Drosophila mauritiana chromosome segments in an otherwise D. sechellia genetic background. We find that recessive hybrid incompatibilities outnumber dominant ones and that hybrid male steriles outnumber all other types of incompatibility, consistent with the dominance and faster-male theories of Haldane's rule, respectively. We also find that, although X-linked and autosomal introgressions are of similar size, most X-linked introgressions cause hybrid male sterility (60%) whereas few autosomal introgressions do (18%). Our results thus confirm the large X effect and identify its proximate cause: incompatibilities causing hybrid male sterility have a higher density on the X chromosome than on the autosomes. We evaluate several hypotheses for the evolutionary cause of this excess of X-linked hybrid male sterility.

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Evolution of Postmating Reproductive Isolation: The Composite Nature of Haldane's Rule and Its Genetic Bases

Cited by 354 publications

References 59 publications

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

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

The costs of being male: are there sex-specific effects of uniparental mitochondrial inheritance?

High-Resolution Genome-Wide Dissection of the Two Rules of Speciation in Drosophila

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