Complex basis of hybrid female sterility and Haldane’s rule inHeliconiusbutterflies: Z-linkage and epistasis

Abstract

Hybrids between diverging populations are often sterile or inviable. Hybrid unfitness usually evolves first in the heterogametic sex -- a pattern known as Haldane's rule. The genetics of Haldane's Rule have been extensively studied in species where the male is the heterogametic (XX/XY) sex, but its basis in taxa where the female is heterogametic (ZW/ZZ), such as Lepidoptera and birds, is largely unknown. Here, we analyse a new case of female hybrid sterility between geographic subspecies of Heliconius pardalinus. The two subspecies mate freely in captivity, but female F1 hybrids in both directions of cross are sterile. Sterility is due to arrested development of oocytes after they become differentiated from nurse cells, but before yolk deposition. We backcrossed fertile male F1 hybrids to parental females, and mapped quantitative trait loci (QTLs) for female sterility. We also identified genes differentially expressed in the ovary, and as a function of oocyte development. The Z chromosome has a major effect, similar to the "large X effect" in Drosophila, with strong epistatic interactions between loci at either end of the Z chromosome, and between the Z chromosome and autosomal loci on chromosomes 8 and 20. Among loci differentially expressed between females with arrested vs. non-arrested ovary development, we identified six candidate genes known also from Drosophila melanogaster and Parage aegeria oogenesis. This study is the first to characterize hybrid sterility using genome mapping in the Lepidoptera. We demonstrate that sterility is produced by multiple complex epistastic interactions often involving the sex chromosome, as predicted by the dominance theory of Haldane's Rule.

Major patterns in the introgression history ofHeliconiusbutterflies

“…In other scenarios, estimated introgression times tend to collapse onto the H. pardalinus-H elevatus divergence time, suggesting that the introgression events were likely misplaced (Figure S17, Table S23). This agrees with the scenario in which H. elevatus is a result of hybrid speciation between H. pardalinus and the common ancestor of the cydno-melpomene clade [42,43].…”

“…In other scenarios, estimated introgression times tend to collapse onto the H. pardalinus-H elevatus divergence time, suggesting that the introgression events were likely misplaced (Figure S18 and Table S23). Our finding that divergence of H. elevatus and introgression from the cydno-melpomene clade occurred almost simultaneously provides evidence for a hybrid speciation origin of H. elevatus resulting from introgression between H. pardalinus and the common ancestor of the cydno-melpomene clade (Rosser et al 2019;Rosser et al 2023).…”

“…We also include introgression between H. besckei and H. numata (b1-n1) to relate the autosome trees to the Zchromosome tree. Finally, sister species H. pardalinus and H. elevatus hybridize today in sympatric populations (Rosser et al 2019;Rosser et al 2023), so we allow introgression between them (p1-e1). According to the 3S analysis, the rates of gene flow in this pair are among the highest (Figure S11).…”

Linkage mapping and genome annotation give novel insights into gene family expansions and regional recombination rate variation in the painted lady (Vanessa cardui) butterfly

“…Under-standing how recombination breaks down linkage disequilibrium between physically linked regions is also important for the efficient design of association studies aimed at coupling genetic variation to phenotypic traits. Despite these important contributions to evolutionary genomics research, detailed recombination maps are only available for a handful of butterfly species (Beldade et al, 2009; Celorio-Mancera et al, 2021; Davey et al, 2017; Rosser et al, 2022; Smolander et al, 2022; Tunström et al, 2021). In some cases, link-age maps have been used to improve and/or verify the correctness of physical genome assemblies, but analysis of the recombination rate has not been thoroughly assessed in many butterfly species.…”

On the impermanence of species: The collapse of genetic incompatibilities in hybridizing populations

“…Recent empirical work on genetic incompatibilities has revealed rather more complex genetic architectures. Incompatibilities in hybrids are generally epistatic, and multiple interacting loci suggest a complex basis of hybrid dysfunction (Courret et al., 2019; Meiklejohn et al., 2018; Rosser et al., 2021). Incompatibilities can also be present as polymorphisms within species (Atlan et al., 2003; Cutter, 2012; Corbett‐Detig et al., 2013; Larson et al., 2018; Zuellig & Sweigart, 2018b).…”