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

ABSTRACT: 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.

SUBMITTER: Sutter A

PROVIDER: S-EPMC3607112 | biostudies-literature | 2013 Apr

REPOSITORIES: biostudies-literature

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

Sutter A A Beysard M M Heckel G G

Heredity 20130123 4

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) ...[more]

PMID: 23340600

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Project description:Over the past half-century, large mammal populations have declined substantially throughout East Africa, mainly due to habitat loss and unsustainable direct exploitation. While it has been acknowledged that the loss of large mammals can have direct and cascading effects on community composition and ecosystem characteristics, limited quantitative work has been done on how declines of large herbivore populations impacts the abundance of mutualistic symbionts. Using a space-for-time observational approach, we quantified the large mammal community alongside the densities, host preferences and behaviors of mutualistic red-billed oxpeckers (Buphagus erythrorhynchus), and yellow-billed oxpeckers (Buphagus africanus) in northern Tanzania. At the landscape scale, mammal community composition was substantially less diverse in highly human-dominated areas when compared with more protected areas, with an observed complete loss of large wild mammal species in two study areas. Mirroring this trend, oxpecker densities were lowest in the least protected areas, and highest in fully protected areas. Using resource selection functions implemented via generalized linear models at different scales, we found that oxpeckers (1) were predominantly (67% of red-billed oxpeckers; 70% of yellow-billed oxpeckers) feeding on larger (between 500kg and 1500kg) ungulate host species within the mammal community, (2) usually preferred feeding on larger individuals (adults and males) within a specific host species population, and (3) preferred hosts that were more tolerant of their presence. In particular, cattle were especially intolerant of oxpecker presence and were relatively effective in displacing oxpeckers. We found little evidence that oxpecker feeding was parasitic across all host species; wound feeding was only observed on giraffe, comprising 6% and 4% of feeding behavior in red-billed and yellow-billed oxpeckers respectively. Thus, a loss of large-bodied and oxpecker tolerant host species is a likely explanation for declines of oxpecker populations in human dominated landscapes, which may have further cascading effects.

Project description:BackgroundHaldane's Rule, the tendency for the heterogametic sex to show reduced fertility in hybrid crosses, can obscure the signal of gene flow in mtDNA between species where females are heterogametic. Therefore, it is important when studying speciation and species limits in female-heterogametic species like birds to assess the signature of gene flow in the nuclear genome as well. We studied introgression of microsatellites and mtDNA across a secondary contact zone between coastal and interior lineages of Western Scrub-Jays (Aphelocoma californica) to test for a signature of Haldane's Rule: a narrower cline of introgression in mtDNA compared to nuclear markers.ResultsOur initial phylogeographic analysis revealed that there is only one major area of contact between coastal and interior lineages and identified five genetic clusters with strong spatial structuring: Pacific Slope, Interior US, Edwards Plateau (Texas), Northern Mexico, and Southern Mexico. Consistent with predictions from Haldane's Rule, mtDNA showed a narrower cline than nuclear markers across a transect through the hybrid zone. This result is not being driven by female-biased dispersal because neutral diffusion analysis, which included estimates of sex-specific dispersal rates, also showed less diffusion of mtDNA. Lineage-specific plumage traits were associated with nuclear genetic profiles for individuals in the hybrid zone, indicating that these differences are under genetic control.ConclusionsThis study adds to a growing list of studies that support predictions of Haldane's Rule using cline analysis of multiple loci of differing inheritance modes, although alternate hypotheses like selection on different mtDNA types cannot be ruled out. That Haldane's Rule appears to be operating in this system suggests a measure of reproductive isolation between the Pacific Slope and interior lineages. Based on a variety of evidence from the phenotype, ecology, and genetics, we recommend elevating three lineages to species level: A. californica (Pacific Slope); A. woodhouseii (Interior US plus Edwards Plateau plus Northern Mexico); A. sumichrasti (Southern Mexico). The distinctive Edwards Plateau population in Texas, which was monophyletic in mtDNA except for one individual, should be studied in greater detail given habitat threat.

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

Publications

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

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