Selective forces in the evolution of gender dimorphism in Lycium (Solanaceae)

Abstract

Explanations for the transition from cosexuality to gender dimorphism have concentrated on overcoming the inherent 50% fitness loss of single-sexed nuclear gene mutants arising in cosexual populations. These mechanisms generally fall into two broad, non-exclusive categories: elimination of inbreeding depression by male-sterile mutants (i.e., selection for outcrossing) and compensatory resource reallocation following loss of one sexual function. This dissertation focuses on the relative importance of these mechanisms in the evolution of gender dimorphism in Lycium (Solanaceae) and then finds an emergent explanation. Plants of North American Lycium californicum, L. exsertum, and L. fremontii are either male-sterile or morphologically hermaphroditic, and populations are gynodioecious. Flowers on hermaphrodites are larger and have broader calyces and corollas than those on females. Phylogenetic relationships, using molecular and morphological data, indicate that gender dimorphism has evolved once in North America and have identified the cosexual relatives of the dimorphic taxa. Controlled pollinations and allozyme estimates of mating systems in cosexual relatives of dimorphic species indicate that gender dimorphism has evolved on a phylogenetic background of self-incompatibility. In contrast, studies of pollen tube growth indicate that hermaphrodites in the dimorphic species are self-compatible. To determine if females compensate for loss of male function, I estimated components of female reproduction for all three dimorphic and three cosexual species. I also investigated reallocation within flowers by quantifying the portion of total floral biomass allocated to each floral whorl. Despite substantial savings due to loss of male function, females do not produce increased numbers of seeds, fruits, or flowers, nor do they allocate additional biomass to gynoecia compared to cosexual relatives. Phylogenetic analysis suggests that the common ancestor of dimorphic Lycium in North America was self-compatible and polyploid. In contrast, relatives of the dimorphic clade are cosexual, self-incompatible diploids. This appears to have occurred independently in African Lycium. I describe a novel hypothesis for the evolution of separate sexes involving polyploidy. In this scenario, polyploidy disrupts self-incompatibility leading to inbreeding depression. Subsequently, male-sterile mutants invade and increase because they are fully outcrossed. Further evidence for this scenario is presented from 12 genera involving at least 20 independent evolutionary events.