Strong asymmetry in the relative strengths of prezygotic and postzygotic barriers between two damselfly sister species

One of the longest debates in biology has been over the relative importance of different isolating barriers in speciation. However, for most species, there are few data evaluating their relative contributions and we can only speculate on the general roles of pre- and postzygotic isolation. Here we quantify the absolute and cumulative contribution of 198 potential reproductive barriers between two sympatric damselfly sister species, Ischnura elegans and I. graellsii, including both premating (habitat, temporal, sexual and mechanical isolation) and postmating barriers (prezygotic: sperm insemination success and removal rate, oviposition success, fertility, fecundity; postzygotic: hybrid viability, hybrid sterility and hybrid breakdown). In sympatry, total reproductive isolation between I. elegans females and I. graellsii males was 95.2%, owing mostly to a premating mechanical incompatibility (93.4%), while other barriers were of little importance. Isolation between I. graellsii females and I. elegans males was also nearly complete (95.8%), which was caused by the cumulative action of multiple prezygotic (n=4, 75.4%) and postzygotic postmating barriers (n=5, 7.4%). Our results suggest that premating barriers are key factors in preventing gene flow between species, and that the relative strengths of premating barriers is highly asymmetrical between the reciprocal crosses.

生物学领域最持久的争论议题之一，聚焦于物种形成过程中各类生殖隔离屏障（reproductive barriers）的相对重要性。然而，针对绝大多数物种，目前尚无足够数据评估各类隔离屏障的相对贡献，我们仅能对合子前隔离与合子后隔离的整体作用进行推测。本研究针对两种同域分布的蟌科姐妹物种——长叶异痣蟌（Ischnura elegans）与格拉夫异痣蟌（I. graellsii），量化了二者之间198种潜在生殖隔离屏障的绝对贡献与累积贡献，涵盖交配前隔离（生境隔离、时间隔离、性隔离与机械隔离）以及交配后隔离；其中交配后隔离又分为合子前隔离（精子授精成功率与移除率、产卵成功率、受精率及繁殖力）与合子后隔离（杂交存活能力、杂交不育及杂交衰退）。在同域分布区域中，长叶异痣蟌雌性与格拉夫异痣蟌雄性之间的总生殖隔离率达95.2%，其核心成因是交配前机械不相容性（占比93.4%），其余隔离屏障的作用可忽略不计。格拉夫异痣蟌雌性与长叶异痣蟌雄性之间的生殖隔离率同样接近完全（95.8%），该隔离由多种合子前隔离（n=4，占比75.4%）与合子后隔离屏障（n=5，占比7.4%）的协同作用所致。本研究结果显示，交配前隔离是阻止物种间基因流的关键因素，且正反交组合间的交配前隔离强度存在显著的不对称性。