The two “rules of speciation” in species with young sex chromosomes

Abstract

The two "rules of speciation," Haldane's rule (HR) and the large-X effect (LXE), are thought to be caused by recessive species incompatibilities exposed in the phenotype due to the hemizygosity of X-linked genes in the heterogametic sex. Thus, the reports of HR and the LXE in species with recently evolved non- or partially degenerate Y-chromosomes, such as Silene latifolia and its relatives, were surprising. Here, I argue that rapid species-specific degeneration of Y-linked genes and associated adjustment of expression of X-linked gametologs (dosage compensation) may lead to rapid evolution of sex-linked species incompatibilities. This process is likely to be too slow in species with old degenerate Y-chromosomes (e.g., in mammals), but Y-degeneration in species with young gene-rich sex chromosomes may be fast enough to play a significant role in speciation. To illustrate this point, I report the analysis of Y-degeneration and the associated evolution of gene expression on the X-chromosome of S. latifolia and Silene dioica, a close relative that shares the same recently evolved sex chromosomes. Despite the recent (≤1MY) divergence of the two species, ~7% of Y-linked genes have undergone degeneration in one but not the other species. This species-specific degeneration appears to drive faster expression divergence of X-linked genes, which may account for HR and the LXE reported for these species. Furthermore, I suggest that "exposure" of autosomal or sex-linked recessive species incompatibilities in the haploid plant gametophyte may mimic the presence of HR in plants. Both haploid expression and species-specific Y-degeneration need to receive more attention if we are to understand the role of these processes in speciation.

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

“…Amphibians carry homomorphic sex chromosomes, but they display ambiguous results (one study complies with the predictions and the other not). The only survey in plants demonstrates that the young X chromosome has an outsized role in speciation, and this may be due to their mechanism of dosage compensation (Filatov, 2018).…”

“Two Rules of Speciation” revisited

“…This grab-bag category includes two unique features of the sex chromosomes: dosage compensation (Johnson & Lachance, 2012), the degeneracy of the Y (or W) chromosome (e.g., Filatov, 2018) or the transcriptional inactivation of the X chromosome during spermatogenesis in some species (Lifschytz & Lindsley, 1972;Presgraves, 2008). Dosage compensation and X inactivation could both be disrupted in hybrids, causing hybrid problems and the appearance of large X effects (disruption of dosage compensation would affect hybrid viability more than fertility).…”

“…There is some evidence for this, including Phadnis and Orr's () demonstration that a gene causing male sterility in D. pseudoobscura USA/Bogota hybrids also causes meiotic drive. Theories based on other special aspects of the sex chromosomes. This grab‐bag category includes two unique features of the sex chromosomes: dosage compensation (Johnson & Lachance, ), the degeneracy of the Y (or W) chromosome (e.g., Filatov, ) or the transcriptional inactivation of the X chromosome during spermatogenesis in some species (Lifschytz & Lindsley, ; Presgraves, ). Dosage compensation and X inactivation could both be disrupted in hybrids, causing hybrid problems and the appearance of large X effects (disruption of dosage compensation would affect hybrid viability more than fertility). The faster evolution of males than females.…”

Introduction: Sex chromosomes and speciation

“…He further argues that the observation of Haldane's rule and/or the large X‐effect in species with young Y chromosomes that have yet to fully degenerate limits the generality of explanations based on hemizygosity. Focusing on two closely related species of the flowering plants, Silene latifolia and Silene doica , with recently evolved sex chromosomes, Filatov () reveals higher divergence in expression at X‐linked gametologs with degenerate Y copies. This finding—the first demonstration of faster‐X expression evolution in plants—indicates that species‐specific degeneration of recently evolved Y chromosomes and compensatory expression evolution of X‐linked gametologs can lead to sex‐linked incompatibilities in hybrids, even on short timescales.…”