Hybrid incompatibilities are affected by dominance and dosage in the haplodiploid wasp Nasonia

Beukeboom, Leo W.; Koevoets, Tosca; Morales, Hernán E.; Ferber, Steven; Zande, Louis van de

doi:10.3389/fgene.2015.00140

Cited by 23 publications

(24 citation statements)

References 62 publications

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“…In the context of hybridization, this means that both beneficial and deleterious recessive allelic combinations are selected more strongly in haploid males than diploid females. In accordance with Haldane's rule (Haldane, ), hybrid breakdown should affect the hemizygous sex (i.e., haploid males) disproportionately, and this has been confirmed by recent studies in haplodiploids (Beukeboom, Koevoets, Morales, Ferber, & van de Zande, ; Koevoets & Beukeboom, ; Kulmuni, Seifert, & Pamilo, ). Hybrid breakdown may be due to failing interactions between two or more nuclear loci (nucleo‐nuclear) or between cytoplasmic and nuclear loci (cytonuclear).…”

Section: Introductionsupporting

confidence: 61%

Widespread hybridization within mound‐building wood ants in Southern Finland results in cytonuclear mismatches and potential for sex‐specific hybrid breakdown

Élias

Pluckrose

et al. 2017

Molecular Ecology

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Hybridization and gene flow between diverging lineages are increasingly recognized as common evolutionary processes, and their consequences can vary from hybrid breakdown to adaptive introgression. We have previously found a population of wood ant hybrids between Formica aquilonia and F. polyctena that shows antagonistic effects of hybridization: females with introgressed alleles show hybrid vigour, whereas males with the same alleles show hybrid breakdown. Here, we investigate whether hybridization is a general phenomenon in this species pair and analyse 647 worker samples from 16 localities in Finland using microsatellite markers and a 1200-bp mitochondrial sequence. Our results show that 27 sampled nests contained parental-like gene pools (six putative F. polyctena and 21 putative F. aquilonia) and all remaining nests (69), from nine localities, contained hybrids of varying degrees. Patterns of genetic variation suggest these hybrids arise from several hybridization events or, instead, have backcrossed to the parental gene pools to varying extents. In contrast to expectations, the mitochondrial haplotypes of the parental species were not randomly distributed among the hybrids. Instead, nests that were closer to parental-like F. aquilonia for nuclear markers preferentially had F. polyctena's mitochondria and vice versa. This systematic pattern suggests there may be underlying selection favouring cytonuclear mismatch and hybridization. We also found a new hybrid locality with strong genetic differences between the sexes similar to those predicted under antagonistic selection on male and female hybrids. Further studies are needed to determine the selective forces that act on male and female genomes in these newly discovered hybrids.

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Section: Introductionsupporting

confidence: 61%

Widespread hybridization within mound‐building wood ants in Southern Finland results in cytonuclear mismatches and potential for sex‐specific hybrid breakdown

Élias

Pluckrose

et al. 2017

Molecular Ecology

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“…By analysing hybrid haploid males from two partially incompatible strains of a haplodiploid mite species, Knegt et al (2017) tested the Bateson-Dobzhansky-Muller model, which emphasizes epistatic interactions between alleles to explain hybrid breakdown, without suffering from the effects of dominance-recessivity hiding epistatic interactions between loci. Also, in some haplodiploid species, it is possible to generate sex-reversed diploid males to unravel dominance and dosage effects in hybrid incompatibility (Beukeboom et al, 2015). Therefore, haplodiploid animals are promising material in the study of evolutionary mechanisms underlying reproductive isolation.…”

Section: Discussionmentioning

confidence: 99%

Patterns of reproductive isolation in a haplodiploid – strong post‐mating, prezygotic barriers among three forms of a social spider mite

Sato

Sakamoto

Gotoh

et al. 2018

J of Evolutionary Biology

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In speciation research, much attention is paid to the evolution of reproductive barriers, preventing diverging groups from hybridizing back into one gene pool. The prevalent view is that reproductive barriers evolve gradually as a by-product of genetic changes accumulated by natural selection and genetic drift in groups that are segregated spatially and/or temporally. Reproductive barriers, however, can also be reinforced by natural selection against maladaptive hybridization. These mutually compatible theories are both empirically supported by studies, analysing relationships between intensity of reproductive isolation and genetic distance in sympatric taxa and allopatric taxa. Here, we present the - to our knowledge - first comparative study in a haplodiploid organism, the social spider mite Stigmaeopsis miscanthi, by measuring premating and post-mating, pre- and post-zygotic components of reproductive isolation, using three recently diverged forms of the mite that partly overlap in home range. We carried out cross-experiments and measured genetic distances (mitochondrial DNA and nuclear DNA) among parapatric and allopatric populations of the three forms. Our results show that the three forms are reproductively isolated, despite the absence of premating barriers, and that the post-mating, prezygotic component contributes most to reproductive isolation. As expected, the strength of post-mating reproductive barriers positively correlated with genetic distance. We did not find a clear pattern of prezygotic barriers evolving faster in parapatry than in allopatry, although one form did show a trend in line with the ecological and behavioural relationships between the forms. Our study advocates the versatility of haplodiploid animals for investigating the evolution of reproductive barriers.

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“…Furthermore, in haplo‐diploid Nasonian wasps genetically engineered diploid males were less affected by hybrid sterility than haploid male hybrids, pointing to a strong effect of ploidy on hybrid fertility (Beukeboom et al. ).…”

Section: Discussionmentioning

confidence: 99%

“…Empirically, hybrid incompatibilities are frequently dosage-sensitive, for example in a Arabidopsis thaliana A. arenosa cross, where a DMI results due to failure in gene silencing (Josefsson et al 2006), or in a Mus musculus musculus M. m. domesticus cross, where X-linked hybrid male sterility results from over-expression of X-linked genes in spermatogenesis (Good et al 2010). Furthermore, in haplo-diploid Nasonian wasps genetically engineered diploid males were less affected by hybrid sterility than haploid male hybrids, pointing to a strong effect of ploidy on hybrid fertility (Beukeboom et al 2015).…”

Section: Of the Modelmentioning

confidence: 99%

Bounds to parapatric speciation: A Dobzhansky-Muller incompatibility model involving autosomes, X chromosomes, and mitochondria

Höllinger

Hermisson

2017

Evolution

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We investigate the conditions for the origin and maintenance of postzygotic isolation barriers, so called (Bateson-)Dobzhansky-Muller incompatibilities or DMIs, among populations that are connected by gene flow. Specifically, we compare the relative stability of pairwise DMIs among autosomes, X chromosomes, and mitochondrial genes. In an analytical approach based on a continent-island framework, we determine how the maximum permissible migration rates depend on the genomic architecture of the DMI, on sex bias in migration rates, and on sex-dependence of allelic and epistatic effects, such as dosage compensation. Our results show that X-linkage of DMIs can enlarge the migration bounds relative to autosomal DMIs or autosome-mitochondrial DMIs, in particular in the presence of dosage compensation. The effect is further strengthened with male-biased migration. This mechanism might contribute to a higher density of DMIs on the X chromosome (large X-effect) that has been observed in several species clades. Furthermore, our results agree with empirical findings of higher introgression rates of autosomal compared to X-linked loci.

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Hybrid incompatibilities are affected by dominance and dosage in the haplodiploid wasp Nasonia

Cited by 23 publications

References 62 publications

Widespread hybridization within mound‐building wood ants in Southern Finland results in cytonuclear mismatches and potential for sex‐specific hybrid breakdown

Widespread hybridization within mound‐building wood ants in Southern Finland results in cytonuclear mismatches and potential for sex‐specific hybrid breakdown

Patterns of reproductive isolation in a haplodiploid – strong post‐mating, prezygotic barriers among three forms of a social spider mite

Bounds to parapatric speciation: A Dobzhansky-Muller incompatibility model involving autosomes, X chromosomes, and mitochondria

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