The historical biogeography of range expansion predicts spatial patterns in reproductive assurance

Abstract

Plant reproductive assurance describes the ability of a plant to successfully reproduce in an environment that is potentially devoid of conspecifics and/or pollinators. Traditionally, studies have focused on the role of contemporary ecology---such as pollinator or mate availability---in driving spatial patterns in reproductive assurance within species, however, historical processes such as post-glacial range expansion may be an understudied alternative explanation for geographic variation in mating system. This is because during the process of geographic range expansion into novel habitat, selection should favour individuals that possess traits promoting reproductive assurance (i.e., autonomous selfing or clonal reproduction). Here, we used Northern pink monkeyflower--Erythranthe (Mimulus lewisii--a hermaphroditic, self-compatible, perennial, alpine plant, as a focal species to investigate the historical signatures of geographic range expansion by combining phylogeographic analyses with a greenhouse survey of range-wide reproductive assurance. First, we detected significant geographic variation among populations in two components of reproductive assurance: self-fertilization and clonal propagation. Next, using genome-wide single nucleotide polymorphism (SNP) data, we identified three distinct genetic clusters structured by longitude and estimated geographic coordinates of the most likely origins of range expansion within each cluster. We found that both measures of reproductive assurance significantly increased on average with distance from the inferred biogeographic origin, which is consistent with the hypothesis that reproductive assurance undergoes adaptive evolution during range expansion. This study supports hypotheses underlying Bakers Law and contributes to our understanding of spatial variation in reproductive assurance, which is linked to variation in evolutionary potential, adaptability, and the long-term persistence of populations across large spatial scales. Lay summaryWhat generates and maintains the amazing diversity in plant reproduction we see today? Traditionally, studies have focused on the role of contemporary ecology, such as pollinator or mate availability, in driving spatial patterns within species, however, historical drivers may be an understudied alternative explanation. Here, we test the hypothesis that expansion into new habitats after glacial retreat, where pollinators or mates were scarce, favors plants with the ability to reproduce in the absence of pollinators and mates by making self-pollinated seeds or vegetative clones of themselves. We find support for the hypothesis, where the probabilities of making both autonomously selfed seed and clonal vegetative propagules increase on average along inferred pathways of range expansion. Our study joins a handful of previous studies that tested and provided support for historical range expansion shaping range-wide spatial variation in reproductive assurance in plants, suggesting post-glacial range expansion may be a common mechanism creating diversity in plant mating systems.