Asymmetric gene flow causes cascading reproductive isolation

Abstract

Hybridization between species can affect the strength of the reproductive barriers that separate those species. Two extensions of this effect are: (1) the expectation that asymmetric hybridization will have asymmetric effects on reproductive barrier strength and (2) the expectation that local hybridization will affect only local reproductive barrier strength and could therefore alter within-species compatibility. We tested these hypotheses in a pair of morning glory species that exhibit asymmetric gene flow from highly selfing Ipomoea lacunosa into mixed mating I. cordatotriloba in regions where they co-occur. Because of the direction of this gene flow, we predicted that reproductive barrier strength would be more strongly affected in I. cordatotriloba than I. lacunosa. We also predicted that changes to reproductive barriers in sympatric I. cordatotriloba populations would affect compatibility with allopatric populations of that species. We tested these predictions by measuring the strength of a reproductive barrier to seed set across the species ranges. Consistent with our first prediction, we found that sympatric and allopatric I. lacunosa produce the same number of seeds in crosses with I. cordatotriloba, whereas crosses between sympatric I. cordatotriloba and I. lacunosa are more successful than crosses between allopatric I. cordatotriloba and I. lacunosa. This difference in compatibility appears to reflect an asymmetric decrease in the strength of the barrier to seed set in sympatric I. cordatotriloba, which could be caused by I. lacunosa alleles that have introgressed into I. cordatotriloba. We further demonstrated that changes to sympatric I. cordatotriloba have decreased its ability to produce seeds with allopatric populations of the same species, in line with our second prediction. Thus, in a manner analogous to cascade reinforcement, we suggest that introgression associated with hybridization not only influences between-species isolation but can also contribute to isolation within a species. Impact StatementBiological diversity depends on traits that prevent different species from successfully interbreeding. However, these reproductive barriers are often imperfect, leading to hybrid matings and possible genetic exchange between species where they occur together. When this happens, the reproductive barriers that separate species can themselves evolve to become stronger or weaker. Understanding the effects of hybridization on reproductive barriers is key to predicting the potential for future hybridization between species and ultimately whether hybridizing species will diverge, persist, or merge in regions where they co-occur. Here we hypothesize and show that hybridization in only one direction causes unidirectional changes to reproductive barrier strength and that geographically restricted hybridization causes local changes to barrier strength that can affect interbreeding within a species. Specifically, we found that gene flow from one species of morning glory into another likely caused a reproductive barrier to decrease in regions where they co-occur. The decreased reproductive barrier is caused by changes in only the species that received gene flow. We also found that the locally reduced barriers in the species that received gene flow affected reproductive compatibility between populations within that species. Thus, a breakdown of barriers between species can cause a build-up of barriers within a species. Our work demonstrates critical and rarely explored interactions at species boundaries.