Evaluating genomic signatures of “the large X‐effect” during complex speciation

Presgraves, Daven C.

doi:10.1111/mec.14777

Cited by 114 publications

(177 citation statements)

References 104 publications

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“…Although introgression within sympatry does not fully explain the observed results, our finding that the sympatric hybrid types (BMs and MBs) consistently differed could be accounted for by differential introgression of the X chromosome in sympatry (Presgraves, ). Differential movement of the X chromosome relative to introgression in the remainder of the genome could also possibly account, at least in part, for the exaggeration (or reduction) of BDMs in sympatric hybrids relative to allopatric hybrids.…”

Section: Discussioncontrasting

confidence: 68%

Variation in hybrid gene expression: Implications for the evolution of genetic incompatibilities in interbreeding species

et al. 2019

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Interbreeding species often produce low‐fitness hybrids due to genetic incompatibilities between parental genomes. Whether these incompatibilities reflect fixed allelic differences between hybridizing species, or, alternatively, standing variants that segregate within them, remains unknown for many natural systems. Yet, evaluating these alternatives is important for understanding the origins and nature of species boundaries. We examined these alternatives using spadefoot toads (genus Spea), which naturally hybridize. Specifically, we contrasted patterns of gene expression in hybrids relative to pure‐species types in experimentally produced tadpoles from allopatric parents versus those from sympatric parents. We evaluated the prediction that segregating variation should result in gene expression differences between hybrids derived from sympatric parents versus hybrids derived from allopatric parents, and found that 24% of the transcriptome showed such differences. Our results further suggest that gene expression in hybrids has evolved in sympatry owing to evolutionary pressures associated with ongoing hybridization. Although we did not measure hybrid incompatibilities directly, we discuss the implications of our findings for understanding the nature of hybrid incompatibilities, how they might vary across populations over time, and the resulting effects on the evolutionary maintenance ‐ or breakdown ‐ of reproductive barriers between species.

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Section: Discussioncontrasting

confidence: 68%

Variation in hybrid gene expression: Implications for the evolution of genetic incompatibilities in interbreeding species

et al. 2019

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“…These results are consistent with growing evidence in many systems that population divergence often proceeds despite on‐going gene flow. This “complex speciation” model implies that different genomic regions, including sex chromosomes, can contribute disproportionately to population differentiation throughout the process of divergence (Presgraves ). We also found evidence for elevated between‐population differentiation on the sex chromosomes compared with autosomes, consistent with observations from several animal taxa (reviewed in Presgraves ).…”

Section: Discussionmentioning

confidence: 99%

“…Analyses of genomic heterogeneity in divergence have often identified sex chromosomes as outliers of differentiation (Presgraves ). This finding is not unexpected: sex chromosomes have long been thought to be associated with speciation (Coyne and Orr 2004).…”

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confidence: 99%

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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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“…; Camus et al. ), while also raising questions about the scope of “faster‐X effects” in adaptive evolution (i.e., the extent to which X‐linked genes diverge more rapidly than autosomal genes during adaptation; Presgraves, , ; Meisel and Connallon ; Lasne et al. ; Charlesworth et al.…”

Section: Discussionmentioning

confidence: 99%

Quantifying the relative contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation*

et al. 2018

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During local adaptation with gene flow, some regions of the genome are inherently more responsive to selection than others. Recent theory predicts that X‐linked genes should disproportionately contribute to local adaptation relative to other genomic regions, yet this prediction remains to be tested. We carried out a multigeneration crossing scheme, using two cline‐end populations of Drosophila melanogaster, to estimate the relative contributions of the X chromosome, autosomes, and mitochondrial genome to divergence in four traits involved in local adaptation (wing size, resistance to heat, desiccation, and starvation stresses). We found that the mitochondrial genome and autosomes contributed significantly to clinal divergence in three of the four traits. In contrast, the X made no significant contribution to divergence in these traits. Given the small size of the mitochondrial genome, our results indicate that it plays a surprisingly large role in clinal adaptation. In contrast, the X, which represents roughly 20% of the Drosophila genome, contributes negligibly—a pattern that conflicts with theoretical predictions. These patterns reinforce recent work implying a central role of mitochondria in climatic adaptation, and suggest that different genomic regions may play fundamentally different roles in processes of divergence with gene flow.

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Evaluating genomic signatures of “the large X‐effect” during complex speciation

Cited by 114 publications

References 104 publications

Variation in hybrid gene expression: Implications for the evolution of genetic incompatibilities in interbreeding species

Variation in hybrid gene expression: Implications for the evolution of genetic incompatibilities in interbreeding species

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

Quantifying the relative contributions of the X chromosome, autosomes, and mitochondrial genome to local adaptation*

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