Data from: Introgression in hybrid ants is favored in females but selected against in males

Hybridization is not a mere reproductive dead end but has been suggested to play a central role in speciation, for example, by introducing adaptive genetic variation. Our previous study uncovered a unique consequence of hybridization in Formica ants. In a population including two isolated but partially introgressed genetic groups, the females have an apparent hybrid background, whereas the males do not. This situation results in large-scale differences between male and female genomes that are stable throughout generations. Here, we compare genotypes from different developmental stages to investigate how sex-specific introgression and genetic differences between sexes are maintained. We show that strong selection rather than sex-dependent transmission maintains the genetic differences between sexes. All genotype combinations are produced and observed in the eggs of both sexes, but the alleles acquired through hybridization disappear from the haploid males during development from egg to adult as their frequencies drop toward zero. However, the same introgressed alleles increase in frequency and are favored when heterozygous in the females. Genotypes eliminated from males most likely represent incompatibilities arising from hybridization. Our results show an unusual situation of opposite selection, where introgression is favored in diploid females but selected against in haploid males. This finding suggests that introgressed genomic regions harbor both fitness-enhancing and -reducing elements. Our work highlights the complex consequences of hybridization and provides a rare opportunity to observe natural selection in real time in nature.

杂交（hybridization）并非仅仅是生殖死胡同，此前研究表明其在物种形成中发挥核心作用，例如通过引入适应性遗传变异。我们的前期研究揭示了蚁属（Formica）蚂蚁中杂交带来的独特后果：在包含两个隔离但存在部分渐渗（introgression）的遗传类群的种群中，雌性个体具有显著的杂交背景，而雄性个体则无此特征。这一情况导致雌雄基因组间出现大规模差异，且该差异可在多代间稳定维持。
本研究通过比较不同发育阶段的基因型，探究性别特异性渐渗及雌雄遗传差异的维持机制。研究显示，维持雌雄遗传差异的并非性别依赖的传递模式，而是强烈的选择压力：在两性的卵中均可产生并观测到所有基因型组合，但杂交引入的等位基因（allele）在单倍体雄性（haploid males）个体从卵发育为成虫的过程中逐渐消失，其频率趋近于零；然而，这类渐渗等位基因在二倍体雌性（diploid females）个体中若呈杂合状态则频率升高并受到正向选择。在雄性个体中被清除的基因型，大概率代表了杂交引发的遗传不相容性。
我们的研究结果展现了一种罕见的反向选择情境：渐渗等位基因在二倍体雌性中受到青睐，却在单倍体雄性中被负向选择。这一发现表明，渐渗的基因组区域同时携带提升适合度（fitness）和降低适合度的遗传元件。本研究凸显了杂交的复杂演化后果，同时为实时观测自然界中的自然选择提供了难得的契机。