The contribution of a pollinator toward plant fitness (i.e., its "effectiveness") can determine its importance for the plant's evolutionary ecology. We compared pollinators in a population of Asclepias incarnata (Apocynaceae) for several components of pollinator effectiveness over two flowering seasons to evaluate their importance to plant reproduction. Insects of the order Hymenoptera predominate in A. incarnata pollination, but there appears to be no specialization for pollination within this order. Pollinators varied significantly in nearly every component of effectiveness that we measured, including pollen load, removal and deposition of pollen, pollination efficiency (deposition/removal), flower-handling time, and potential for geitonogamy (fractional pollen deposition). The visitation rate of pollinators also varied significantly between years and through time within years. Pollination success and percentage fruit-set of unmanipulated plants in the population also varied significantly between years, and pollination success varied among sample times within years. Most components of effectiveness were weakly correlated, suggesting that the contributions of visitor species toward pollination varied among effectiveness components. Mean flower-handling time, however, was strongly correlated with several components, including pollen removal and deposition, pollination efficiency, and fractional pollen deposition. These findings highlight the significance of pollination variability for plant reproduction and suggest that time-dependent foraging behaviors may play an important role in determining pollinator effectiveness.

Most models of mating system evolution predict mixed mating to be unstable, although it is commonly reported from nature. Ecological interactions with mutualistic pollinators can help account for this discrepancy, but antagonists such as herbivores are also likely to play a role. In addition, inbreeding can alter ecological interactions and directly affect selfing rates, which may also contribute to maintaining mating system variation. We explored herbivore and inbreeding effects on pollinator behavior and selfing rates in Mimulus guttatus. First, individual spittlebug (Philaenus spumarius) herbivores were applied to native plants in two populations. Spittlebugs reduced flower size, increased anther-stigma distance, and increased selfing rates. A second experiment factorially crossed spittlebug treatment with inbreeding history (self- vs. cross-fertilized), using potted plants in arrays. Spittlebugs did not affect pollinator behavior, but they reduced flower size and nearly doubled the selfing rate. Inbreeding reduced the frequency of pollinator visits and increased flower-handling time, and this may be the first report that inbreeding affects pollinator behavior. Selfing rates of inbred plants were reduced by one half, which may reflect early inbreeding depression or altered pollinator behavior. The contrasting effects of herbivory and inbreeding on selfing rates may help maintain mating system variation in M. guttatus.

Inbreeding, which is common in plants, may increase the vulnerability of populations to natural enemies. Similarly, natural enemies may increase the expression of inbreeding depression in their hosts, resulting in altered selection on host mating-system evolution. To examine effects of inbreeding on tolerance to herbivory, we transplanted experimentally self-and cross-fertilized plants into four field populations of Mimulus guttatus and applied single Philaenus spumarius (spittlebug) nymphs to half. At the end of the growing season, we scored plants for five fitness components (reproductive effort, biomass, survival, probability of producing flowers or buds, and probability of bolting). Inbreeding reduced population-level tolerance to spittlebug herbivory with respect to plant aboveground biomass. Inbreeding effects on tolerance varied significantly among plant families for three fitness traits, indicating the opportunity for selection by herbivores to improve tolerance in inbreeding populations. These results also indicate that herbivores can alter inbreeding depression in plants. Our results mirror earlier greenhouse studies of inbreeding effects on plant-herbivore interactions, and demonstrate that these effects can be manifested in natural settings as well. This study indicates that inbreeding in natural populations can affect fitness not only directly, but also indirectly through altered interactions with natural enemies.

In this Viewpoint paper we highlight three important themes that span and integrate different subdisciplines: the changes in morphology, phenology, and physiology that accompany the transition to selfing; the evolutionary consequences of pollen pool diversity in flowering plants; and the evolutionary dynamics of sexual polymorphisms. We also highlight recent developments in molecular techniques that will facilitate more efficient and cost-effective study of mating patterns in large natural populations, research on the dynamics of pollen transport, and investigations on the genetic basis of sexual polymorphisms. This Viewpoint also serves as the introduction to a Special Issue on the Evolution of Plant Mating Systems. The 15 papers in this special issue provide inspiring examples of recent discoveries, and glimpses of exciting developments yet to come.

The hypothesis that plant mating systems may evolve indirectly via selection on correlated life history characteristics is plausible and warrants increased attention.