Molecular signatures of long-distance oceanic dispersal and the colonization of Pacific islands in Lycium carolinianum.

Abstract

Long-distance dispersal has been important in explaining the present distributions of many plant species. Despite being infrequent, such dispersal events have considerable evolutionary consequences, because bottlenecks during colonization can result in reduced genetic diversity. We examined the phylogeographic history of Lycium carolinianum, a widespread taxon that ranges from southeastern North America to several Pacific islands, with intraspecific diversity in sexual and mating systems. We used Bayesian, likelihood, and coalescent approaches with nuclear and plastid sequence data and genome-wide single nucleotide polymorphisms to reconstruct the dispersal history of this species. We also compared patterns of genetic variation in mainland and island populations using single nucleotide polymorphisms and allelic diversity at the S-RNase mating system gene. Lycium carolinianum is monophyletic and dispersed once from the North American mainland, colonizing the Pacific islands ca. 40,100 years ago. This dispersal was accompanied by a loss of genetic diversity in SNPs and the S-RNase locus due to a colonization bottleneck and the loss of self-incompatibility. Additionally, we documented at least two independent transitions to gynodioecy: once following the colonization of the Hawaiian Islands and loss of self-incompatibility, and a second time associated with polyploidy in the Yucatán region of Mexico. Long-distance dispersal via fleshy, bird dispersed fruits best explains the unusually widespread distribution of L. carolinianum. The collapse of diversity at the S-RNase locus in island populations suggests that self-fertilization may have facilitated the subsequent colonization of Pacific islands following a single dispersal from mainland North America.