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Restricted X chromosome introgression and support for Haldane's rule in hybridizing damselflies.

ABSTRACT: Contemporary hybrid zones act as natural laboratories for the investigation of species boundaries and may shed light on the little understood roles of sex chromosomes in species divergence. Sex chromosomes are considered to function as a hotspot of genetic divergence between species; indicated by less genomic introgression compared to autosomes during hybridization. Moreover, they are thought to contribute to Haldane's rule, which states that hybrids of the heterogametic sex are more likely to be inviable or sterile. To test these hypotheses, we used contemporary hybrid zones of Ischnura elegans, a damselfly species that has been expanding its range into the northern and western regions of Spain, leading to chronic hybridization with its sister species Ischnura graellsii. We analysed genome-wide SNPs in the Spanish I. elegans and I. graellsii hybrid zone and found (i) that the X chromosome shows less genomic introgression compared to autosomes, and (ii) that males are underrepresented among admixed individuals, as predicted by Haldane's rule. This is the first study in Odonata that suggests a role of the X chromosome in reproductive isolation. Moreover, our data add to the few studies on species with X0 sex determination system and contradict the hypothesis that the absence of a Y chromosome causes exceptions to Haldane's rule.

SUBMITTER: Swaegers J

PROVIDER: S-EPMC9297008 | biostudies-literature | 2022 Jul

REPOSITORIES: biostudies-literature

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Restricted X chromosome introgression and support for Haldane's rule in hybridizing damselflies.

Swaegers Janne J Sánchez-Guillén Rosa Ana RA Chauhan Pallavi P Wellenreuther Maren M Hansson Bengt B

Proceedings. Biological sciences 20220720 1979

Contemporary hybrid zones act as natural laboratories for the investigation of species boundaries and may shed light on the little understood roles of sex chromosomes in species divergence. Sex chromosomes are considered to function as a hotspot of genetic divergence between species; indicated by less genomic introgression compared to autosomes during hybridization. Moreover, they are thought to contribute to Haldane's rule, which states that hybrids of the heterogametic sex are more likely to b ...[more]

PMID: 35855603

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Project description:BackgroundStudying contemporary hybridization increases our understanding of introgression, adaptation and, ultimately, speciation. The sister species Ischnura elegans and I. graellsii (Odonata: Coenagrionidae) are ecologically, morphologically and genetically similar and hybridize. Recently, I. elegans has colonized northern Spain, creating a broad sympatric region with I. graellsii. Here, we review the distribution of both species in Iberia and evaluate the degree of introgression of I. graellsii into I. elegans using six microsatellite markers (442 individuals from 26 populations) and five mitochondrial genes in sympatric and allopatric localities. Furthermore, we quantify the effect of hybridization on the frequencies of the genetically controlled colour polymorphism in females of both species.ResultsIn a principal component analysis of the microsatellite data, the first two principal components summarised almost half (41%) of the total genetic variation. The first axis revealed a clear separation of I. graellsii and I. elegans populations, while the second axis separated I. elegans populations. Admixture analyses showed extensive hybridization and introgression in I. elegans populations, consistent with I. elegans backcrosses and occasional F1-hybrids, suggesting hybridization is on-going. More specifically, approximately 58% of the 166 Spanish I. elegans individuals were assigned to the I. elegans backcross category, whereas not a single of those individuals was assigned to the backcross with I. graellsii. The mitochondrial genes held little genetic variation, and the most common haplotype was shared by the two species.ConclusionsThe results suggest rapid species turnover in sympatric regions in favour of I. elegans, corroborating previous findings that I. graellsii suffers a mating disadvantage in sympatry with I. elegans. Examination of morph frequency dynamics indicates that hybridization is likely to have important implications for the maintenance of multiple female morphs, in particular during the initial period of hybridization.

Project description:BackgroundThe nematode Pristionchus pacificus has been developed as a satellite organism in evolutionary developmental biology for comparison to Caenorhabditis elegans. Comparative studies have revealed major differences in the regulation of developmental processes between P. pacificus and C. elegans. To place evolutionary developmental biology and the observed developmental differences between species in a comprehensive evolutionary context, such studies have to be complemented with ecological aspects. Knowledge about the ecology of the organism in question might indicate specific environmental conditions that can result in developmental adaptations and could account for species differences in development. To this end, we have started to investigate the ecology of Pristionchus nematodes. In recent field studies in Western Europe we found six Pristionchus species that are closely associated with scarab beetles and the Colorado potato beetle. This Pristionchus-beetle association provides the unique opportunity to combine research in evolutionary developmental biology with ecology. However, it remains unknown how general these findings from Europe are on a global scale.ResultsHere, we describe the Pristionchus species associated with scarab and Colorado potato beetles in the Eastern United States and show striking transatlantic differences and unexpected evolutionary and ecological patterns. Two hundred eighty of 285 (98%) isolates from American scarab beetles belong to five Pristionchus species, all of which are different from the European species. We describe four of them as novel Pristionchus species. The five American Pristionchus species fall into a single phylogenetic clade and have a male-female (gonochoristic) mode of reproduction, whereas the majority of European isolates are hermaphroditic. Crosses between the two most closely related species, P. aerivorus and P. pseudaerivorus n. sp., follow Haldane's rule in that heterogametic F1 males are inviable. We observed P. aerivorus and P. pseudaerivorus n. sp. coexisting on the same scarab beetle and obtained two cases of F1 hybrids from wild beetles. Finally, the Colorado potato beetle is associated with the same nematode, P. uniformis in the United States and Europe. Given the introduction of the Colorado potato beetle to Europe in 1877, our results suggest that P. uniformis was introduced together with its beetle vector.ConclusionTaken together, the Pristionchus-beetle association provides a powerful tool for studying biodiversity, biogeography, speciation and species invasion on a global scale.

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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Restricted X chromosome introgression and support for Haldane's rule in hybridizing damselflies.

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Restricted X chromosome introgression and support for Haldane's rule in hybridizing damselflies.

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