Patterns of Hybrid Seed Inviability in the Mimulus guttatus sp. Complex Reveal a Potential Role of Parental Conflict in Reproductive Isolation

Genomic conflicts may play a central role in the evolution of reproductive barriers. Theory predicts that early-onset hybrid inviability may stem from conflict between parents for resource allocation to offspring. Here, we describe M. decorus: a group of cryptic species within the M. guttatus species complex that are largely reproductively isolated by hybrid seed inviability (HSI). HSI between M. guttatus and M. decorus is common and strong, but populations of M. decorus vary in the magnitude and directionality of HSI with M. guttatus. Patterns of HSI between M. guttatus and M. decorus, as well as within M. decorus, conform to the predictions of parental conflict: first, reciprocal F1s exhibit size differences and parent-of-origin-specific endosperm defects; second, the extent of asymmetry between reciprocal F1 seed size is correlated with asymmetry in HSI; and third, inferred differences in the extent of conflict predict the extent of HSI between populations. We also find that HSI is rapidly evolving, as populations that exhibit the most HSI are each others’ closest relative. Lastly, although all populations appear largely outcrossing, we find that the differences in the inferred strength of conflict scale positively with π, suggesting that demographic or life history factors other than transitions to self-fertilization may influence the rate of parental-conflict-driven evolution. Overall, these patterns suggest the rapid evolution of parent-of-origin-specific resource allocation alleles coincident with HSI within and between M. guttatus and M. decorus. Parental conflict may therefore be an important evolutionary driver of reproductive isolation. [Display omitted] •Mimulus decorus is a cryptic species complex within the M. guttatus species complex•M. decorus is reproductively isolated from M. guttatus by hybrid seed inviability•Patterns of hybrid seed inviability conform to the predictions of parental conflict•Differences in conflict between species scale with genome-wide diversity Genomic conflict may play a central role in speciation. Coughlan et al. find that parental conflict may play a role in the evolution of hybrid seed inviability between Mimulus guttatus and a newly discovered species complex M. decorus. Differences in conflict between these lineages may stem from demographic or life history differences.