Abstract:
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 in Papilio and Heliconius butterflies 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.
Notes:
Xiong, Tianzhu Tarikere, Shreeharsha Rosser, Neil Li, Xueyan Yago, Masaya Mallet, James eng Internal Funding/Harvard University Department of Organismic and Evolutionary Biology/ 1764269/The Quantitative Biology Initiatives at Harvard; The NSF-Simons Center for Mathematical and Statistical Analysis of Biology at Harvard/ Grant in Aid of Research/Sigma Xi, The Scientific Research Honor Society/ 32070482/National Natural Science Foundation of China/ 21H02215/JSPS KAKENHI Grant/ 2023/10/19 Proc Natl Acad Sci U S A. 2023 Oct 31;120(44):e2300959120. doi: 10.1073/pnas.2300959120. Epub 2023 Oct 19.
Website
