Did sex chromosome turnover promote divergence of the major mammal groups?

Graves, Jennifer A. Marshall

doi:10.1002/bies.201600019

Cited by 53 publications

(42 citation statements)

References 85 publications

(95 reference statements)

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“…In addition, comparative genomic studies of sterilizing and nonsterilizing mitochondrial genomes that co-occur in a given species have shown that sterilizing genomes exhibit a higher rate of evolution (Darracq et al 2010(Darracq et al , 2011. As dioecy and sex-chromosomes have been suggested to drive speciation rates (Käfer et al 2014;Graves 2016), gynodioecy could reveal itself to be another reproductive system that facilitates reproductive isolation and thus speciation in a very effective way, in a tempo faster than phenotypic diversification (Orr 1995), resulting in cryptic species. Therefore, we expect that the accumulation of mutations in the mitochondrial genome occurs independently in the two S. nutans lineages and would ultimately induce reproductive isolation through cytonuclear genetic incompatibilities.…”

Section: Discussionmentioning

confidence: 99%

Lineages ofSilene nutansdeveloped rapid, strong, asymmetric postzygotic reproductive isolation in allopatry

et al. 2017

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Reproductive isolation can rise either as a consequence of genomic divergence in allopatry or as a byproduct of divergent selection in parapatry. To determine whether reproductive isolation in gynodioecious Silene nutans results from allopatric divergence or from ecological adaptation following secondary contact, we investigated the pattern of postzygotic reproductive isolation and hybridization in natural populations using two phylogeographic lineages, western (W1) and eastern (E1). Experimental crosses between the lineages identified strong, asymmetric postzygotic isolation between the W1 and the E1 lineages, independent of geographic overlap. The proportion of ovules fertilized, seeds aborted, and seeds germinated revealed relatively little effect on the fitness of hybrids. In contrast, hybrid mortality was high and asymmetric: while half of the hybrid seedlings with western lineage mothers died, nearly all hybrid seedlings with E1 mothers died. This asymmetric mortality mirrored the proportion of chlorotic seedlings, and is congruent with cytonuclear incompatibility. We found no evidence of hybridization between the lineages in regions of co-occurrence using nuclear and plastid markers. Together, our results are consistent with the hypothesis that strong postzygotic reproductive isolation involving cytonuclear incompatibilities arose in allopatry. We argue that the dynamics of cytonuclear gynodioecy could facilitate the evolution of reproductive isolation.

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Section: Discussionmentioning

confidence: 99%

Lineages ofSilene nutansdeveloped rapid, strong, asymmetric postzygotic reproductive isolation in allopatry

et al. 2017

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“…Such fusions are easily recognizable because they cause an odd number of chromosomes in a diploid karyotype of one sex and might be implicated with speciation (e.g. [50, 52, 53]). In A. burtoni , males and females have the same karyotype of 2n = 40 ([12], personal communication with Cesar Martins) indicating that chromosome fusions were not causing the formation of neo-sex chromosomes.…”

Section: Discussionmentioning

confidence: 99%

Variations on a theme: Genomics of sex determination in the cichlid fish Astatotilapia burtoni

et al. 2016

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BackgroundSex chromosomes change more frequently in fish than in mammals or birds. However, certain chromosomes or genes are repeatedly used as sex determinants in different members of the teleostean lineage. East African cichlids are an enigmatic model system in evolutionary biology representing some of the most diverse extant vertebrate adaptive radiations. How sex is determined and if different sex-determining mechanisms contribute to speciation is unknown for almost all of the over 1,500 cichlid species of the Great Lakes. Here, we investigated the genetic basis of sex determination in a cichlid from Lake Tanganyika, Astatotilapia burtoni, a member of the most species-rich cichlid lineage, the haplochromines.ResultsWe used RAD-sequencing of crosses for two populations of A. burtoni, a lab strain and fish caught at the south of Lake Tanganyika. Using association mapping and comparative genomics, we confirmed male heterogamety in A. burtoni and identified different sex chromosomes (LG5 and LG18) in the two populations of the same species. LG5, the sex chromosome of the lab strain, is a fusion chromosome in A. burtoni. Wnt4 is located on this chromosome, representing the best candidate identified so far for the master sex-determining gene in our lab strain of A. burtoni.ConclusionsCichlids exemplify the high turnover rate of sex chromosomes in fish with two different chromosomes, LG5 and LG18, containing major sex-determining loci in the two populations of A. burtoni examined here. However, they also illustrate that particular chromosomes are more likely to be used as sex chromosomes. Chromosome 5 is such a chromosome, which has evolved several times as a sex chromosome, both in haplochromine cichlids from all Great Lakes and also in other teleost fishes.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3178-0) contains supplementary material, which is available to authorized users.

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“…First, rearrangements involving sex chromosomes may be implicated in driving divergence between populations in the same manner as other chromosomal rearrangements, as outlined above (reviewed in Connallon et al 2018). Second, sex chromosome turnover may cause imbalance in the sex determination process of hybrids, resulting in hybrid infertility and therefore increasing divergence between populations with different sex chromosome systems (Haldane 1922;Dobzhansky 1937;Graves 2016). For both of these reasons, sex chromosome turnover may be a particularly important driver of population divergence and speciation.…”

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Ancestral and neo‐sex chromosomes contribute to population divergence in a dioecious plant

2019

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Empirical evidence from several animal groups suggests sex chromosomes disproportionately contribute to reproductive isolation. This effect may be enhanced when sex chromosomes are associated with turnover of sex determination systems resulting from structural rearrangements to the chromosomes. We investigated these predictions in the dioecious plant Rumex hastatulus, which is composed of populations of two different sex chromosome cytotypes caused by an X‐autosome fusion. Using population genomic analyses, we investigated the demographic history of R. hastatulus and explored the contributions of ancestral and neo‐sex chromosomes to population genetic divergence. Our study revealed that the cytotypes represent genetically divergent populations with evidence for historical but not contemporary gene flow between them. In agreement with classical predictions, we found that the ancestral X chromosome was disproportionately divergent compared with the rest of the genome. Excess differentiation was also observed on the Y chromosome, even when we used measures of differentiation that control for differences in effective population size. Our estimates of the timing of the origin of neo‐sex chromosomes in R. hastatulus are coincident with cessation of gene flow, suggesting that the chromosomal fusion event that gave rise to the origin of the XYY cytotype may have also contributed to reproductive isolation.

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Did sex chromosome turnover promote divergence of the major mammal groups?

Cited by 53 publications

References 85 publications

Lineages ofSilene nutansdeveloped rapid, strong, asymmetric postzygotic reproductive isolation in allopatry

Lineages ofSilene nutansdeveloped rapid, strong, asymmetric postzygotic reproductive isolation in allopatry

Variations on a theme: Genomics of sex determination in the cichlid fish Astatotilapia burtoni

Ancestral and neo‐sex chromosomes contribute to population divergence in a dioecious plant

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