Keller Barbara, de Vos Jurriaan M, Schmidt-Lebuhn Alexander N, Thomson James D, Conti Elena
Department of Systematic and Evolutionary Botany University of Zürich Zollikerstrasse 107 8008 Zürich Switzerland.
Department of Ecology and Evolutionary Biology Brown University 80 Waterman Street Box G-W Providence Rhode Island 02912 USA; Present address: Comparative Plant and Fungal Biology Department Royal Botanic Gardens Kew Richmond Surrey TW9 3AE UK.
Ecol Evol. 2016 Aug 4;6(17):6223-44. doi: 10.1002/ece3.2293. eCollection 2016 Sep.
The interaction between floral traits and reproductive isolation is crucial to explaining the extraordinary diversity of angiosperms. Heterostyly, a complex floral polymorphism that optimizes outcrossing, evolved repeatedly and has been shown to accelerate diversification in primroses, yet its potential influence on isolating mechanisms remains unexplored. Furthermore, the relative contribution of pre- versus postmating barriers to reproductive isolation is still debated. No experimental study has yet evaluated the possible effects of heterostyly on pre- and postmating reproductive mechanisms. We quantify multiple reproductive barriers between the heterostylous Primula elatior (oxlip) and P. vulgaris (primrose), which readily hybridize when co-occurring, and test whether traits of heterostyly contribute to reproductive barriers in unique ways. We find that premating isolation is key for both species, while postmating isolation is considerable only for P. vulgaris; ecogeographic isolation is crucial for both species, while phenological, seed developmental, and hybrid sterility barriers are also important in P. vulgaris, implicating sympatrically higher gene flow into P. elatior. We document for the first time that, in addition to the aforementioned species-dependent asymmetries, morph-dependent asymmetries affect reproductive barriers between heterostylous species. Indeed, the interspecific decrease of reciprocity between high sexual organs of complementary floral morphs limits interspecific pollen transfer from anthers of short-styled flowers to stigmas of long-styled flowers, while higher reciprocity between low sexual organs favors introgression over isolation from anthers of long-styled flowers to stigmas of short-styled flowers. Finally, intramorph incompatibility persists across species boundaries, but is weakened in long-styled flowers of P. elatior, opening a possible backdoor to gene flow through intramorph pollen transfer between species. Therefore, patterns of gene flow across species boundaries are likely affected by floral morph composition of adjacent populations. To summarize, our study highlights the general importance of premating isolation and newly illustrates that both morph- and species-dependent asymmetries shape boundaries between heterostylous species.
花部性状与生殖隔离之间的相互作用对于解释被子植物的非凡多样性至关重要。花柱异长是一种复杂的花部多态现象，可优化异交，它多次进化，并且已被证明能加速报春花的多样化，但它对隔离机制的潜在影响仍未得到探索。此外，交配前障碍与交配后障碍对生殖隔离的相对贡献仍存在争议。尚无实验研究评估花柱异长对交配前和交配后生殖机制的可能影响。我们对花柱异长的高报春（高报春）和报春花（报春花）之间的多种生殖障碍进行了量化，这两种植物共存时很容易杂交，并测试花柱异长的性状是否以独特方式促成生殖障碍。我们发现，交配前隔离对两个物种都很关键，而交配后隔离仅对报春花很重要；生态地理隔离对两个物种都至关重要，而物候、种子发育和杂种不育障碍在报春花中也很重要，这意味着同域情况下有更高的基因流向高报春。我们首次证明，除了上述物种依赖性不对称外，形态依赖性不对称也影响花柱异长物种之间的生殖障碍。实际上，互补花形态的高性器官之间种间互作的减少限制了种间花粉从短花柱花的花药转移到长花柱花的柱头，而低性器官之间更高的互作则有利于从长花柱花的花药到短花柱花的柱头的渐渗而非隔离。最后，形态内不亲和性跨越物种边界持续存在，但在高报春的长花柱花中减弱，为通过物种间形态内花粉转移实现基因流动打开了一个可能的后门。因此，跨物种边界的基因流动模式可能受相邻种群的花形态组成影响。总之，我们的研究突出了交配前隔离的普遍重要性，并新说明了形态依赖性和物种依赖性不对称都塑造了花柱异长物种之间的边界。
