Mate choice driven by genome in an allopolyploid fish complex

Nonsexual complexes which lack typical reproductive isolation and show multiple conspecific and heterospecific mating options among hybrids and parental species are excellent models to study mate choice based on genetics. The allopolyploid fish complex Squalius alburnoides includes multiple fertile male and female genomotypes reproducing among each other and with the sympatric bisexual species of the Squalius genus. We used this hybridogenetic complex to study the relationship between mate preference and mates’ genetic background, focusing on a population whose mating options include two bisexual Squalius species. The preference of S. alburnoides hybrid females towards multiple male genomotypes was assessed in affiliation trials, and the levels of admixture between the genomes of the two bisexual Squalius species were measured using next-generation genotyping. The genome of the most recent Squalius species in the drainage was admixed with variable genetic portions typically allocated to the other species, but not the opposite, suggesting that the newer species in the drainage may be more prone to interspecific crosses. Female mate preferences were related to males’ genetic background, but also to the genetic background of the choosy female itself. Overall, females showed higher preference towards males with admixed genomes over pure males, and towards males with a genetic background more similar to their own. This trend favors crosses between the hybrids and the most recent bisexual Squalius species in the drainage, promoting the flow of its genome into the hybridogenetic complex. These findings highlight an intricate interplay between mate choice and mates’ genomes, which may be directly related to genetic benefits.

缺乏典型生殖隔离、且在杂种与亲本物种间存在多种同物种及异物种交配选择的无性复合体，是开展基于遗传学的配偶选择研究的绝佳模型。异源多倍体鱼类复合体（Squalius alburnoides）包含多个可育的雄性与雌性基因组型，这些基因组型可彼此交配，也可与同域分布的真白鱼属双性物种进行繁殖。本研究以该杂种生殖复合体为对象，探究配偶偏好与配偶遗传背景之间的关联，重点关注一个同时存在两种真白鱼属双性物种作为交配选择对象的种群。
研究人员通过亲和性试验，评估了S. alburnoides杂种雌性对多种雄性基因组型的偏好，并借助下一代基因分型技术，测定了这两种真白鱼属双性物种的基因组混合程度。研究发现，该水系中最晚出现的真白鱼物种基因组携带着通常归属于另一物种的可变遗传片段，反之则不成立，这表明该水系中的较新物种更易发生种间杂交。
雌性的配偶偏好不仅与雄性的遗传背景相关，同时也与择偶雌性自身的遗传背景有关。总体而言，雌性对携带混合基因组的雄性的偏好程度高于纯合雄性，且更倾向于选择遗传背景与自身更为相似的雄性。
这一趋势有利于杂种与该水系中最晚出现的真白鱼属双性物种之间的交配，进而推动该物种的基因组向杂种生殖复合体中流动。本研究结果揭示了配偶选择与配偶基因组之间复杂的相互作用，而这种相互作用可能直接与遗传收益相关。