The rates of introgression and barriers to genetic exchange between hybridizing species: sex chromosomes vs. autosomes

Abstract

Interspecific crossing experiments have shown that sex chromosomes play a major role in the reproductive isolation of many species. However, their ability to act as reproductive barriers, which hamper interspecific genetic exchange, has hardly been evaluated quantitatively in relation to autosomes. Yet, this genome-wide limitation of gene flow is essential for understanding the complete separation of species, and thus speciation. Here, we develop a mainland-island model of secondary contact between hybridizing species of a XY (or ZW) sexual system. We obtain theoretical predictions for the frequency of introgressed alleles, and the strength of the barrier to neutral gene flow of the two types of chromosomes carrying multiple interspecific barrier loci. Theoretical predictions are obtained for scenarios where introgressed alleles are rare. We show that the same analytical expressions apply for sex chromosomes and autosomes, but with different effective parameters. The specific features of sex chromosomes (hemizygosity and absence of recombination in the heterogametic sex) lead to reduced levels of introgression of the X (or Z) compared to autosomes. This effect is enhanced by certain types of dosage compensation or sex-biased forces; but it remains overall small (except when incompatibilities are recessive). We discuss these predictions in light of empirical data comprising model-based tests of introgression and dine surveys in various biological systems.

Faster-haplodiploid evolution under divergence-with-gene-flow: simulations and empirical data from pine-feeding hymenopterans

“…This mechanism produces faster-X differentiation at neutral sites linked to both recessive and codominant alleles, with faster-X differentiation most pronounced in the recessive case (Figure 5B). These results are also consistent with predictions from deterministic continent-island models of secondary-contact (Fusco and Uyenoyama 2011;Muirhead and Presgraves 2016;Fraïsse and Sachdeva 2021). Despite several important differences between our model and these secondary contact models, including divergence scenario, migration direction, and the presence of drift, we reach qualitatively similar conclusions.…”

“…First, the genetic architecture of adaptation to novel niches is likely much more complex (i.e., many loci with variable effect sizes, dominance coefficients, and non-additive interactions) than the simple single-locus model considered here. Although there has been some work on how divergent selection on multiple, possibly interacting, loci impacts genomic differentiation (e.g., (Yeaman et al 2016;Aeschbacher et al 2017)), this has not been investigated in the context of hemizygosity (but see (Fusco and Uyenoyama 2011;Fraïsse and Sachdeva 2021)). Second, the model we considered was also relatively simple, ignoring sex-specific effects such as sex-biased migration, sex-specific selection, and the absence of dosage compensation.…”

“…To date, several theoretical studies have explored how gene flow under different demographic histories, selection regimes, and genome features affect genetic variants linked to locally maladapted immigrant loci, ultimately shaping genome-wide patterns of genetic differentiation (Petry 1983;Barton and Bengtsson 1986;Charlesworth et al 1997;Feder and Nosil 2010;Jeffrey L. Feder et al 2012;Cruickshank and Hahn 2014;Yeaman et al 2016;Aeschbacher et al 2017;Ravinet et al 2017;Matthey-Doret and Whitlock 2019). However, hemizygosity has been largely ignored in this context, and the few studies that have addressed the effects of linked selection at hemizygous loci with migration focused on scenarios of secondary contact between fully differentiated species, investigating the impact of incompatibilities (Fusco and Uyenoyama 2011;Muirhead and Presgraves 2016;Fraïsse and Sachdeva 2021). To our knowledge, the effects of linked selection at hemizygous loci have not been examined under scenarios of divergence with gene flow driven by divergent selection.…”

A genetic switch for male UV-iridescence in an incipient species pair of sulphur butterflies

“…The large 5′ intergenic and intronic regions of bab in Colias and Ostrinia, and of its sub-functionalized duplicates in Drosophila, together suggest a complex cis-regulatory landscape bearing a multitude of enhancers or silencers (47)(48)(49), enabling the evolution of precise, tissue-specific changes (50). Last, the location of Bab on the lepidopteran Z chromosome is relevant to the divergence of premating traits under the assumption that sex-chromosomes are more prone to the generation of reproductive isolation than autosomes (20,51,52). These possible generative biases will require further investigation among diverged Drosophila species, as well as in the Colias UV display and Ostrinia mate detection systems.…”

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

“…The heterogeneity of genomic divergence is expected to be the result of the interplay between natural and sexual selection as well as gene flow, demography and recombination. However, characterizing the genomic architecture of barriers to gene exchange remains a key challenge in studies of speciation (Payseur and Rieseberg 2016;Fraïsse and Sachdeva 2020), especially in non-model species (Fraïsse and Sachdeva 2020).…”