Evolution of Dioecy in Echinocereus coccineus: Relative Influence of Pollinators, Resources and Elevation over Multiple Spatial Scales

of a dissertation at the University of Miami. Dissertation supervised by Professor Theodore H. Fleming. Number of pages in text. (176) “Why have separate sexes? ” is a fundamental biological question that has been investigated intensively since Darwin first proposed two alternative hypotheses: Separate sexes evolve 1) to avoid the detrimental effects of self-fertilization or 2) to improve the allocation of scarce resources to each sex’s reproductive function. In animal-pollinated plants these two hypotheses have been invoked to explain why: 1) dioecy is strongly associated with small, generalized pollinators. Dioecy is hypothesized to evolve because this type of pollinator produces high rates of self-fertilization, and separation of the sexes avoids this inbreeding. It has also been hypothesized that: 2) dioecy may evolve primarily because this allows plants to optimize the different ways resources are used for the dissemination (male) and collection (female) of pollen. I concurrently tested these two hypotheses using Echinocereus coccineus (Cactaceae), a perennial tetraploid (2n = 44) cactus that blooms throughout the mountains of the southwestern United States. It has a variable mating system across its range: populations in the high-elevation center are hermaphroditic, while populations at the low-elevation edges of the range are dioecious. Both pollinators (hummingbirds vs. bees) and amount of resources (rainfall) varied across this range. This allowed me to test the relative influence of pollinator type and resource gradients on the evolution of dioecy. I found that, as predicted, when specialized pollinators (hummingbirds) were excluded from plants and only generalized pollinators (bees) visited, the selfing rate of plants increased 238%. This combination of high selfing rates and high levels of inbreeding depression found in E. coccineus populations could select for dioecy, even in the absence of resource reallocation by the plants. Besides maintaining high outcrossing rates within populations, hummingbirds may also maintain high levels of gene flow among E. coccineus populations: Synchronously blooming populations whose phenologies coincided with the hummingbird migration through this area had lower FST values (i.e. less genetic divergence) than populations with asynchronous phenologies, or those that bloomed after the hummingbird migration had passed by. Population inbreeding (FIS) was not correlated with pollinator visit rates. Instead, it was negatively correlated with elevation. This could indicate that inbred progeny are selected against at higher rates in cold, highelevation environments. These population genetic data suggest that the frequency of dioecious populations should be negatively correlated with both hummingbird abundance and elevation. Structural equation models of the effects of hummingbird abundance, elevation and annual rainfall (resources) on dioecy across the range of E. coccineus supported this hypothesis. Across all models, elevation, rainfall, and hummingbird abundance were consistently negatively correlated with dioecy; meaning that dioecy is more likely to be found as each of these variables decline. Only models with hummingbird abundance as a direct predictor of dioecy significantly fit the data. Models with only resources as a predictor of dioecy did not fit the data. This allowed me to reject hypothesis 2 for the evolution of dioecy: In this system resource reallocation does not appear to be important because there is no correlation between resources and dioecy. Darwin’s first hypothesis is supported: as hummingbird abundance declines (and selfing rates increase), the incidence of dioecious populations increases. Finally, to determine how changes in pollinator type may be globally influencing the evolution of dioecy, I conducted a literature survey of change in pollinator types along elevation gradients and compared these to studies of dioecy along elevation gradients. Across studies the trend was clear: specialized insect pollinators decline with elevation, leaving only generalized pollinators (usually flies) at the highest elevations. Along with this pattern, proportion of dioecious species in communities (or proportion of single-sex mutants in a population) increases with elevation. In cases of vertebratepollinated plants (e.g. those pollinated by birds and/or bats), dioecy is predicted to evolve at lower elevations because these specialized pollinators often occur at middle to high elevations, leaving lower elevations to generalized pollinators. The E. coccineus study system fits this prediction. I propose that elevation may be useful as a worldwide predictor of dioecy due to its effects on pollinator community composition and amount of inbreeding depression expressed in plant populations as elevation increases. The research presented in this dissertation represents the first study to concurrently test the inbreeding avoidance and resource allocation hypotheses for the evolution of dioecy. It was also the first to show that a change in pollinators across the range of an ancestrally hermaphroditic plant species could cause sufficient selection on hermaphrodite individuals to promote the selection for separate sexes and eventually allow the evolution of dioecy in populations. Predictions formulated by this study will be used in future work to test how changes in pollinators along elevation gradients may influence the evolution of dioecy around the world.