Sex-specific population structure, natural selection, and linkage disequilibrium in a wild bird population as revealed by genome-wide microsatellite analyses

Li, Menghua; Merilä, Juha

doi:10.1186/1471-2148-10-66

Cited by 14 publications

(9 citation statements)

References 67 publications

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“…This is particularly true for haplodiploids, which display about 2-3 times the LD of the diploid model with the same parameters. Transferred to the context of X/Z chromosomes, this is consistent with observations of larger LD on the X chromosome as compared with autosomes (Wall et al, 2002; Sandor et al, 2006; Li and Merilä, 2010). It has been argued that this is because selection is more effective on X-linked loci: recessive deleterious mutations are more visible to selection in haploid individuals (Charlesworth et al, 1987).…”

Section: Discussionsupporting

confidence: 85%

Conflict between heterozygote advantage and hybrid incompatibility in haplodiploids (and sex chromosomes)

Ghenu

Blanckaert

Butlin

et al. 2017

Preprint

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1In many diploid species the sex chromosomes play a special role in mediating reproductive 2 isolation. In haplodiploids (i.e., females are diploid and males haploid), the whole genome 3 behaves similar to the X/Z chromosomes of diploids, and thus haplodiploid systems can serve 4 as a model for the role of sex chromosomes in speciation and hybridization. A previously 5 described population of Finnish Formica wood ants displays genome-wide signs of ploidally 6 and sexually antagonistic selection resulting from hybridization. Here, hybrid diploid females 7 have increased survivorship but hybrid haploid males are inviable. In order to understand how 8 this unusual natural population may sustain this antagonistic selection for hybrid status, we 9 developed a mathematical model with hybrid incompatibility, female heterozygote advantage, 10 1 recombination, and assortative mating. The rugged fitness landscape resulting from the 11 conflict between heterozygote advantage and hybrid incompatibility results in sexual conflict 12 in haplodiploids, which is absent in diploids. Thus, whereas heterozygote advantage always 13 promotes long-term polymorphism in diploids, we find various outcomes in haplodiploids 14 in which the conflict can be resolved either in favor of males, females, or via maximizing 15 the number of introgressed individuals. We fit our model to data from the Finnish wood 16 ant population in order to discuss its potential long-term fate. We highlight the general 17 implications of our results for speciation and hybridization in haplodiploids versus diploids, 18 and how such fitness conflicts could contribute to the outstanding role of sex chromosomes 19 as hotspots of sexual conflict and genes involved in speciation. 20Introduction 21 Haplodiploids are an emerging system for speciation genetics (Koevoets and Beukeboom, 22 2009; Kulmuni and Pamilo, 2014; Lohse and Ross, 2015; Knegt et al., 2017). Although ≈ 20% 23 of animal species are haplodiploid (comprising most Hymenopterans, some arthropods, thrips 24 and Hemipterans, and several clades of beetles and mites; Crozier and Pamilo, 1996; Evans 25 et al., 2004; de la Filia et al., 2015), little evolutionary theory has been developed specifically 26 for speciation in haplodiploids (Koevoets and Beukeboom, 2009). Under haplodiploidy with 27 arrhenotoky (hereafter simply haplodiploidy; Suomalainen et al., 1987), males develop from 28 the mother's unfertilized eggs and are haploid, whereas eggs fertilized by fathers result in 29 diploid females. Since this mode of inheritance is from a theoretical viewpoint similar to 30 that of the X/Z chromosome, most work on speciation of haplodiploids comes from the rich 31 literature of sex chromosome evolution (Jablonka and Lamb, 1991; Presgraves, 2008; Johnson 32 and Lachance, 2012; Lohse and Ross, 2015). An important similarity between haplodiploids 33 and X/Z chromosomes is that recessive mutations in the haploid sex are exposed to selec-34 tion, but they are masked in diploids. Thi...

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Section: Discussionsupporting

confidence: 85%

Conflict between heterozygote advantage and hybrid incompatibility in haplodiploids (and sex chromosomes)

Ghenu

Blanckaert

Butlin

et al. 2017

Preprint

View full text Add to dashboard Cite

show abstract

“…This is particularly true for haplodiploids, which display about 2–3 times the LD of the diploid model with the same parameters. Transferred to the context of X/Z chromosomes, this is consistent with observations of larger LD on the X chromosome as compared with autosomes (Li & Merilä, ; Sandor et al., ; Wall, Andolfatto, & Przeworski, ). It has been argued that this is because selection is more effective on X‐linked loci: recessive deleterious mutations are more visible to selection in haploid individuals (Charlesworth et al., ).…”

Section: Discussionsupporting

confidence: 85%

Conflict between heterozygote advantage and hybrid incompatibility in haplodiploids (and sex chromosomes)

et al. 2018

View full text Add to dashboard Cite

In many diploid species, the sex chromosomes play a special role in mediating reproductive isolation. In haplodiploids, where females are diploid and males haploid, the whole genome behaves similarly to the X/Z chromosomes of diploids. Therefore, haplodiploid systems can serve as a model for the role of sex chromosomes in speciation and hybridization. A previously described population of Finnish Formica wood ants displays genome-wide signs of ploidally and sexually antagonistic selection resulting from hybridization. Here, hybrid females have increased survivorship but hybrid males are inviable. To understand how the unusual hybrid population may be maintained, we developed a mathematical model with hybrid incompatibility, female heterozygote advantage, recombination and assortative mating. The rugged fitness landscape resulting from the co-occurrence of heterozygote advantage and hybrid incompatibility results in a sexual conflict in haplodiploids, which is caused by the ploidy difference. Thus, whereas heterozygote advantage always promotes long-term polymorphism in diploids, we find various outcomes in haplodiploids in which the population stabilizes either in favour of males, females or via maximizing the number of introgressed individuals. We discuss these outcomes with respect to the potential long-term fate of the Finnish wood ant population and provide approximations for the extension of the model to multiple incompatibilities. Moreover, we highlight the general implications of our results for speciation and hybridization in haplodiploids versus diploids and how the described fitness relationships could contribute to the outstanding role of sex chromosomes as hotspots of sexual antagonism and genes involved in speciation.

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“…Although deviations from HWE or distortion from linkage equilibrium might be a random effect associated with the sample size and/or level of marker polymorphism, these two features combined may indicate some population distortion. In general, the high levels of linkage disequilibrium and deviation from HWE in populations are associated with small effective population size, significant intrapopulation genetic structure, and occurrence of inbreeding (Li and Merilä 2010). Given the fact that the Isfjorden and Kongsfjorden colonies are among the smallest in the Svalbard area, it is possible that the observed deviations reflect ongoing demographic processes in these two populations.…”

Section: Discussionmentioning

confidence: 99%

Weak population genetic differentiation in the most numerous Arctic seabird, the little auk

et al. 2014

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Quantifying patterns of genetic diversity and differentiation among populations of Arctic birds is fundamental for understanding past and ongoing population processes in the Arctic. However, the genetic differentiation of many important Arctic species remains uninvestigated. Here, phylogeography and population genetics were examined in the worldwide population of a small seabird, the little auk (dovekie, Alle alle)-the most numerous avian species of the Arctic ecosystem. Blood samples or feathers were collected from 328 little auks (325 from the nominate subspecies and 3 from the A. a. polaris) in nine main breeding aggregations in the northern Atlantic and one location from the Pacific Ocean. The mtDNA haplotypes of the two subspecies were not segregated into separate groups. Also, no genetic structure was found within the nominate race based on microsatellite markers. The level of genetic differentiation among populations was low yet significant (mean F ST = 0.005). Some pairwise F ST comparisons revealed significant differences, including those involving the most distant Pacific colony as well as among some Atlantic populations. Weak population differentiation following the model of isolation by distance in the little auk is similar to the patterns reported in other highArctic bird species, indicating that a lack of distinct genetic structure is a common phenomenon in the Arctic avifauna.

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Sex-specific population structure, natural selection, and linkage disequilibrium in a wild bird population as revealed by genome-wide microsatellite analyses

Cited by 14 publications

References 67 publications

Conflict between heterozygote advantage and hybrid incompatibility in haplodiploids (and sex chromosomes)

Conflict between heterozygote advantage and hybrid incompatibility in haplodiploids (and sex chromosomes)

Conflict between heterozygote advantage and hybrid incompatibility in haplodiploids (and sex chromosomes)

Weak population genetic differentiation in the most numerous Arctic seabird, the little auk

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