Genetic Analysis of Autosomal and X-Linked Markers Across a Mouse Hybrid Zone

Macholán, Miloš; Munclinger, Pavel; Šugerková, Monika; Dufková, Petra; Bímová, Barbora Vošlajerová; Božíková, Eva; Zima, Jan; Piálek, Jaroslav

doi:10.1111/j.1558-5646.2007.00065.x

Cited by 214 publications

(291 citation statements)

References 128 publications

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“…Furthermore, a balance between gene flow and selection against hybrids often leads to the formation of narrow hybrid zones, reducing recombination and therefore allowing divergence between populations either side of the zone to continue (parapatric speciation; Kondrashov, 2003). Clines of sex-linked loci are often narrower than those of autosomal loci, for example in the house mouse (Tucker et al, 1992;Dod et al, 1993Dod et al, , 2005Raufaste et al, 2005;Macholán et al, 2007), indicating either that selection against hybrids is more efficient on the X/Z chromosome or that it is more likely to contain genes selected against in hybrids. Either way, recombination in parapatry is lower for X/Z-linked loci than autosomal loci, increasing their potential for divergence.…”

Section: Evolution Of Genetic Incompatibilitymentioning

confidence: 99%

Speciation through evolution of sex-linked genes

2008

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Identification of genes involved in reproductive isolation opens novel ways to investigate links between stages of the speciation process. Are the genes coding for ecological adaptations and sexual isolation the same that eventually lead to hybrid sterility and inviability? We review the role of sex-linked genes at different stages of speciation based on four main differences between sex chromosomes and autosomes; (1) relative speed of evolution, (2) non-random accumulation of genes, (3) exposure of incompatible recessive genes in hybrids and (4) recombination rate. At early stages of population divergence ecological differences appear mainly determined by autosomal genes, but fastevolving sex-linked genes are likely to play an important role for the evolution of sexual isolation by coding for traits with sex-specific fitness effects (for example, primary and secondary sexual traits). Empirical evidence supports this expectation but mainly in female-heterogametic taxa. By contrast, there is clear evidence for both strong X-and Z-linkage of hybrid sterility and inviability at later stages of speciation. Hence genes coding for sexual isolation traits are more likely to eventually cause hybrid sterility when they are sex-linked. We conclude that the link between sexual isolation and evolution of hybrid sterility is more intuitive in male-heterogametic taxa because recessive sexually antagonistic genes are expected to quickly accumulate on the X-chromosome. However, the broader range of sexual traits that are expected to accumulate on the Z-chromosome may facilitate adaptive speciation in female-heterogametic species by allowing male signals and female preferences to remain in linkage disequilibrium despite periods of gene flow.

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Section: Evolution Of Genetic Incompatibilitymentioning

confidence: 99%

Speciation through evolution of sex-linked genes

2008

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“…2007; Macholán et al. 2007), while exogenous selection operates via organismal adaptation to external environments (Vines et al. 2003; Dodd and Afzal‐Rafii 2004; Nosil et al.…”

Section: Introductionmentioning

confidence: 99%

Ecological differentiation and habitat unsuitability maintaining a ground beetle hybrid zone

Yasuda

Osawa

2015

Ecology and Evolution

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Exogenous selection via interactions between organisms and environments may influence the dynamics of hybrid zones between species in multiple ways. Two major models of a hybrid zone allowed us to hypothesize that environmental conditions influence hybrid zone dynamics in two ways. In the first model, an environmental gradient determines the mosaic distribution at the boundary between ecologically differentiated species (mosaic hybrid zone model). In the second model, a patch of unsuitable habitat traps a hybrid zone between species whose hybrids are unfit (tension zone model). To test these, we examined the environmental factors influencing the spatial structure of a hybrid zone between the ground beetles Carabus maiyasanus and C. iwawakianus using GIS‐based quantification of environmental factors and a statistical comparison of species distribution models (SDMs). We determined that both of the hypothetical processes can be important in the hybrid zone. We detected interspecific differences in the environmental factors in presence localities and their relative contribution in SDMs. SDMs were not identical between species even within contact areas, but tended to be similar within the range of each species. These results suggest an association between environments and species, and provide evidence that ecological differentiation between species plays a role in the maintenance of the hybrid zone. Contact areas were characterized by a relatively high temperature, low precipitation, and high topological wetness. Thus, the contact areas were regarded as being located in an unsuitable habitat with a drier climate, where those populations are likely to occur in patches with limited precipitation concentrated. A comparison of spatial scales suggests that exogenous selection via environmental factors may be weaker than endogenous selection via genitalic incompatibility.

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“…For example, in the European hybrid zone between M. m. musculus and M. m. domesticus (diverged 4700 000 generations ago; She et al, 1990) the transition of sex chromosomes is similar in width to M. arvalis (for example, o4 km) and mtDNA clines are also wider (for example, Dod et al, 1993;Raufaste et al, 2005;Macholan et al, 2007;. This is likely a consequence of Haldane's rule in place in the hybrid zone, which may-among other factors-prevent the mouse Y-chromosome cline width to increase (Britton-Davidian et al, 2005; but see Turner et al, 2012).…”

Section: Evidence For Selectionmentioning

confidence: 99%

“…Incomplete reproductive isolation is often characterized by sex-specific processes, and in particular intrinsic genetic incompatibilities often more strongly affect hybrids of the heterogametic sex, a pattern known as Haldane's rule (Haldane, 1922;Schilthuizen et al, 2011). One expectation from Haldane's rule is that the extent of gene flow between incipient species may strongly differ if a gene is paternally or maternally transmitted (Turelli and Begun, 1997;Coyne and Orr, 2004;Macholan et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…The exploration of this contact zone has shown, for example, that the subspecies may mate assortatively (Ganem et al, 2008), hybrids may differ from parentals in parasite load (see Baird et al, 2012) or male hybrids may be sterile (reviewed in Britton-Davidian et al, 2005; and also Mihola et al, 2009). The observation of male sterility combined with the detection of abrupt Y-and X-chromosome marker clines (Dod et al, 1993;Macholan et al, 2007; relative to other markers across the hybrid zone are consistent with the hypothesis that sex chromosomes and in particular factors on the X-chromosome have an important role in causing genetic incompatibilities in mouse hybrids (Coyne and Orr, 2004). Nevertheless, there is extensive geographical and individual variation in male sterility (BrittonDavidian et al, 2005;Good et al, 2008;Turner et al, 2012), and sex-chromosomal marker clines may be not coincident with other genetic markers in particular geographical regions, potentially due to asymmetrical processes (Macholan et al, 2008;Jones et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Sex-specific clines support incipient speciation in a common European mammal

2013

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Hybrid zones provide excellent opportunities to study processes and mechanisms underlying reproductive isolation and speciation. Here we investigated sex-specific clines of molecular markers in hybrid zones of morphologically cryptic yet genetically highly-diverged evolutionary lineages of the European common vole (Microtus arvalis). We analyzed the position and width of four secondary contact zones along three independent transects in the region of the Alps using maternally (mitochondrial DNA) and paternally (Y-chromosome) inherited genetic markers. Given male-biased dispersal in the common vole, a selectively neutral secondary contact would show broader paternal marker clines than maternal ones. In a selective case, for example, involving a form of Haldane's rule, Y-chromosomal clines would not be expected to be broader than maternal markers because they are transmitted by the heterogametic sex and thus gene flow would be restricted. Consistent with the selective case, paternal clines were significantly narrower or at most equal in width to maternal clines in all contact zones. In addition, analyses using maximum likelihood cline-fitting detected a shift of paternal relative to maternal clines in three of four contact zones. These patterns suggest that processes at the contact zones in the common vole are not selectively neutral, and that partial reproductive isolation is already established between these evolutionary lineages. We conclude that hybrid zone movement, sexual selection and/or genetic incompatibilities are likely associated with an unusual unidirectional manifestation of Haldane's rule in this common European mammal.

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Genetic Analysis of Autosomal and X-Linked Markers Across a Mouse Hybrid Zone

Cited by 214 publications

References 128 publications

Speciation through evolution of sex-linked genes

Speciation through evolution of sex-linked genes

Ecological differentiation and habitat unsuitability maintaining a ground beetle hybrid zone

Sex-specific clines support incipient speciation in a common European mammal

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