Colonization, Baker's law, and the evolution of gynodioecy in Hawaii: implications from a study of Lycium carolinianum

Abstract

Premise: As Baker's law suggests, the successful colonization of oceanic islands is often associated with uniparental reproduction (self-fertility), but the high incidence of dimorphism (dioecy, gynodioecy) on islands complicates this idea. Lycium carolinianum is widespread, occurring on the North American mainland and the Hawaiian Islands. We examined Baker's ideas for mainland and island populations of L. carolinianum and examined inbreeding depression as a possible contributor to the evolution of gynodioecy on Maui.

Methods: Controlled crosses were conducted in two mainland populations and two populations in Hawaii. Treatments included self and cross pollination, unmanipulated controls, and autogamy/agamospermy. Alleles from the self-incompatibility S-RNase gene were isolated and compared between mainland and island populations. Given self-compatibility in Hawaii, we germinated seeds from self- and cross- treatments and estimated inbreeding depression using seven traits and a measure of cumulative fitness.

Results: Mainland populations of Lycium carolinianum are predominately self-incompatible with some polymorphism for self-fertility, whereas Hawaiian populations are self-compatible. Concordantly, S-RNase allelic diversity is reduced in Hawaii compared to the mainland. Hawaiian populations also exhibit significant inbreeding depression.

Conclusions: Self-compatibility in Hawaii and individual variation in self-fertility in mainland populations suggests that a colonization filter promoting uniparental reproduction may be acting in this system. Comparison of S-RNase variation suggests a collapse of allelic diversity and heterozygosity at the S-RNase locus in Hawaii, which likely contributed to mate limitation upon arrival to the Pacific. Inbreeding depression coupled with autonomous self-fertilization may have led to the evolution of gynodioecy on Maui.

Keywords: Lycium carolinianum; Baker's law, gametophytic self-incompatibility; Hawaii, inbreeding depression, Lycium; Solanaceae; gynodioecy; male-sterility; self-compatibility.