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Two robust rules have been discovered about animal hybrids: Heterogametic hybrids are more unfit (Haldane’s rule), and sex chromosomes are disproportionately involved in hybrid incompatibility (the large-X/Z effect). The exact mechanisms causing these rules in female heterogametic taxa such as butterflies are unknown but are suggested by theory to involve dominance on the sex chromosome. We investigate hybrid incompatibilities adhering to both rules inPapilioandHeliconiusbutterflies and show that dominance theory cannot explain our data. Instead, many defects coincide with unbalanced multilocus introgression between the Z chromosome and all autosomes. Our polygenic explanation predicts both rules because the imbalance is likely greater in heterogametic females, and the proportion of introgressed ancestry is more variable on the Z chromosome. We also show that mapping traits polygenic on a single chromosome in backcrosses can generate spurious large-effect QTLs. This mirage is caused by statistical linkage among polygenes that inflates estimated effect sizes. By controlling for statistical linkage, most incompatibility QTLs in our hybrid crosses are consistent with a polygenic basis. Since the two genera are very distantly related, polygenic hybrid incompatibilities are likely common in butterflies.
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This content will become publicly available on December 1, 2025
Y chromosome introgression between deeply divergent primate species
Abstract Hybridization and introgression are widespread in nature, with important implications for adaptation and speciation. Since heterogametic hybrids often have lower fitness than homogametic individuals, a phenomenon known as Haldane’s rule, loci inherited strictly through the heterogametic sex rarely introgress. We focus on the Y-chromosomal history of guenons, African primates that hybridized extensively in the past. Although our inferences suggest that Haldane’s rule generally applies, we uncover a Y chromosome introgression event between two species ca. six million years after their initial divergence. Using simulations, we show that selection likely drove the introgressing Y chromosome to fixation from a low initial frequency. We identify non-synonymous substitutions on the novel Y chromosome as candidate targets of selection, and explore meiotic drive as an alternative mechanism. Our results provide a rare example of Y chromosome introgression, showing that the ability to produce fertile heterogametic hybrids likely persisted for six million years in guenons.
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- Award ID(s):
- 1718715
- PAR ID:
- 10572546
- Publisher / Repository:
- Nature Portfolio
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 15
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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