Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Biological Intelligence, Seewiesen, Germany.
Biodiversity Research Institute (CSIC, Oviedo University, Principality of Asturias), University of Oviedo, Mieres, Spain.
J Anim Ecol. 2023 Aug;92(8):1639-1657. doi: 10.1111/1365-2656.13961. Epub 2023 May 25.
All animals host a microbial community within and on their reproductive organs, known as the reproductive microbiome. In free-living birds, studies on the sexual transmission of bacteria have typically focused on a few pathogens instead of the bacterial community as a whole, despite a potential link to reproductive function. Theory predicts higher sexual transmission of the reproductive microbiome in females via the males' ejaculates and higher rates of transmission in promiscuous systems. We studied the cloacal microbiome of breeding individuals of a socially polyandrous, sex-role-reversed shorebird, the red phalarope (Phalaropus fulicarius). We expected (i) higher microbial diversity in females compared to males; (ii) low compositional differentiation between sexes; (iii) lower variation in composition between individuals (i.e. microbiome dispersion) in females than in males; (iv) convergence in composition as the breeding season progresses as a consequence of sexual transmission and/or shared habitat use; and (v) higher similarity in microbial composition between social pair members than between two random opposite-sex individuals. We found no or small between-sex differences in cloacal microbiome diversity/richness and composition. Dispersion of predicted functional pathways was lower in females than in males. As predicted, microbiome dispersion decreased with sampling date relative to clutch initiation of the social pair. Microbiome composition was significantly more similar among social pair members than among two random opposite-sex individuals. Pair membership explained 21.5% of the variation in taxonomic composition and 10.1% of functional profiles, whereas temporal and sex effects explained only 0.6%-1.6%. Consistent with evidence of functional convergence of reproductive microbiomes within pairs, some select taxa and predicted functional pathways were less variable between social pair members than between random opposite-sex individuals. As predicted if sexual transmission of the reproductive microbiome is high, sex differences in microbiome composition were weak in a socially polyandrous system with frequent copulations. Moreover, high within-pair similarity in microbiome composition, particularly for a few taxa spanning the spectrum of the beneficial-pathogenic axis, demonstrates the link between mating behaviour and the reproductive microbiome. Our study is consistent with the hypothesis that sexual transmission plays an important role in driving reproductive microbiome ecology and evolution.
所有动物的生殖器官内和表面都存在微生物群落，即生殖微生物组。在自由生活的鸟类中，关于细菌的性传播的研究通常集中在少数几种病原体上，而不是整个细菌群落，尽管这与生殖功能有潜在联系。理论预测，雌性通过雄性的精液更有可能传播生殖微生物组，在滥交系统中传播速度更高。我们研究了社会性多配偶制、性别反转的滨鸟红杓鹬（Phalaropus fulicarius）繁殖个体的泄殖腔微生物组。我们预期：(i) 与雄性相比，雌性的微生物多样性更高；(ii) 两性之间的组成差异较低；(iii) 与雄性相比，雌性个体之间的组成变化（即微生物组离散度）较低；(iv) 随着繁殖季节的进展，由于性传播和/或共享栖息地的使用，组成趋于一致；(v) 社会对成员之间的微生物组成比两个随机异性个体之间更相似。我们发现泄殖腔微生物组多样性/丰富度和组成在两性之间没有或只有很小的差异。与雄性相比，预测功能途径的离散度在雌性中较低。正如预测的那样，随着与社会对繁殖开始的时间间隔，微生物组离散度下降。社会对成员之间的微生物组成明显比两个随机异性个体之间更相似。对成员身份解释了分类组成的 21.5%和功能谱的 10.1%的变化，而时间和性别效应仅解释了 0.6%-1.6%。与生殖微生物组在对内功能趋同的证据一致，一些选择的分类群和预测的功能途径在社会对成员之间的变化比在随机异性个体之间的变化更小。如果生殖微生物组的性传播很高，那么在一个频繁交配的社会性多配偶制系统中，微生物组组成的性别差异较弱，这与预测相符。此外，对微生物组组成的高度相似性，特别是跨越有益-致病轴谱的少数分类群，证明了交配行为与生殖微生物组之间的联系。我们的研究与性传播在驱动生殖微生物组生态和进化中发挥重要作用的假设一致。
