David A. Moeller

Plant mating systems in a changing world

There is increasing evidence that human disturbance can negatively impact plant-pollinator interactions such as outcross pollination. We present a meta-analysis of 22 studies involving 27 plant species showing a significant reduction in the proportion of seeds outcrossed in response to anthropogenic habitat modifications. We discuss the evolutionary consequences of disturbance on plant mating systems, and in particular whether reproductive assurance through selfing effectively compensates for reduced outcrossing. The extent to which disturbance reduces pollinator versus mate availability could generate diverse selective forces on reproductive traits. Investigating how anthropogenic change influences plant mating will lead to new opportunities for better understanding of how mating systems evolve, as well as of the ecological and evolutionary consequences of human activities and how to mitigate them.

FACILITATIVE INTERACTIONS AMONG PLANTS VIA SHARED POLLINATORS

Outcrossing in plants is influenced by the availability of pollinators and compatible mates, both of which may be modified by the population and community context in which plant–pollinator interactions occur. Although indirect interactions among plants through shared pollinators are often expected to be competitive, pollinator sharing may be beneficial when plant species jointly attract or maintain populations of pollinators. In this study, I tested the hypothesis that pollinator-sharing congeners facilitate reproduction in a focal taxon, Clarkia xantiana ssp. xantiana, and that positive interactions are most pronounced in small and sparse populations. Population surveys revealed that C. x. xantiana frequently coexists with pollinator-sharing congeners except at the periphery of its range. Populations varied extensively in size and density, with small populations more likely associated with pollinator-sharing congeners; conversely, populations occurring alone were more likely large. Flowering schedules in...

ECOLOGICAL CONTEXT OF THE EVOLUTION OF SELF-POLLINATION IN CLARKIA XANTIANA: POPULATION SIZE, PLANT COMMUNITIES, AND REPRODUCTIVE ASSURANCE

Abstract The repeated evolutionary transition from outcrossing to self‐pollination in flowering plants has been suggested to occur because selfing provides reproductive assurance. Reports from biogeographical and ecological surveys indicate that selfing taxa are often associated with stressful and ephemeral environments, situations in which plant abundance is low (e.g., Bakers law) and with novel plant communities, however experimental tests of ecological hypotheses are few. In this study, we examined the ecological context of selection on mating system traits (herkogamy and protandry) in a California annual, Clarkia xantiana, where natural selfing populations differ from outcrossing populations in that they are often of small size or low density and occur mainly outside the range of pollinator‐sharing congeners. We constructed artificial populations of plants with broad genetic variation in floral traits and manipulated two ecological factors, plant population size, and the presence versus absence of pollinator‐sharing congeners, in the center of the geographic range of outcrossing populations. We found evidence for context‐dependent selection on herkogamy and protandry via female fitness in which reduced traits, which promote autonomous selfing, were favored in small populations isolated from congeners whereas selection was comparatively weak in large populations or when congeners were present. In small, isolated populations, the fertility of plants with low herkogamy or protandry was elevated by 66% and 58%, respectively, compared to those with high herkogamy or protandry. The presence of pollinator‐sharing congeners augmented bee visitation rates to C. xantiana flowers by 47% for all bees and by 93% for pollen specialists. By facilitating pollinator visitation, congeners mitigated selection on mating system traits in small populations, where outcross mating success is often low (the Allee effect). We also found support for the hypothesis that pollinator availability directly influenced variation in the strength of selection on herkogamy among populations. The striking parallels between our experimental results and patterns of variation in ecological factors across the geographic range of outcrossing and selfing populations suggest that reproductive assurance may play a central role in directing mating system evolution in C. xantiana.

Correlated evolution of mating system and floral display traits in flowering plants and its implications for the distribution of mating system variation

Reduced allocation to structures for pollinator attraction is predicted in selfing species. We explored the association between outcrossing and floral display in a broad sample of angiosperms. We used the demonstrated relationship to test for bias against selfing species in the outcrossing rate distribution, the shape of which has relevance for the stability of mixed mating. Relationships between outcrossing rate, flower size, flower number and floral display, measured as the product of flower size and number, were examined using phylogenetically independent contrasts. The distribution of floral displays among species in the outcrossing rate database was compared with that of a random sample of the same flora. The outcrossing rate was positively associated with the product of flower size and number; individually, components of display were less strongly related to outcrossing. Compared with a random sample, species in the outcrossing rate database showed a deficit of small floral display sizes. We found broad support for reduced allocation to attraction in selfing species. We suggest that covariation between mating systems and total allocation to attraction can explain the deviation from expected trade-offs between flower size and number. Our results suggest a bias against estimating outcrossing rates in the lower half of the distribution, but not specifically against highly selfing species.

Analysis of Inbreeding Depression in Mixed-Mating Plants Provides Evidence for Selective Interference and Stable Mixed Mating

Hermaphroditic individuals can produce both selfed and outcrossed progeny, termed mixed mating. General theory predicts that mixed‐mating populations should evolve quickly toward high rates of selfing, driven by rapid purging of genetic load and loss of inbreeding depression (ID), but the substantial number of mixed‐mating species observed in nature calls this prediction into question. Lower average ID reported for selfing than for outcrossing populations is consistent with purging and suggests that mixed‐mating taxa in evolutionary transition will have intermediate ID. We compared the magnitude of ID from published estimates for highly selfing (r > 0.8), mixed‐mating (0.2 ≤r≥ 0.8), and highly outcrossing (r < 0.2) plant populations across 58 species. We found that mixed‐mating and outcrossing taxa have equally high average lifetime ID (δ= 0.58 and 0.54, respectively) and similar ID at each of four life‐cycle stages. These results are not consistent with evolution toward selfing in most mixed‐mating taxa. We suggest that prevention of purging by selective interference could explain stable mixed mating in many natural populations. We identify critical gaps in the empirical data on ID and outline key approaches to filling them.

Pollinator community structure and sources of spatial variation in plant–pollinator interactions in Clarkia xantiana ssp. xantiana

The structure of diverse floral visitor assemblages and the nature of spatial variation in plant–pollinator interactions have important consequences for floral evolution and reproductive interactions among pollinator-sharing plant species. In this study, I use surveys of floral visitor communities across the geographic range of Clarkia xantiana ssp. xantiana (hereafter C. x. xantiana) (Onagraceae) to examine the structure of visitor communities, the specificity of the pollination system, and the role of variation in the abiotic vs. biotic environment in contributing to spatial variation in pollinator abundance and community composition. Although the assemblage of bee visitors to C. x. xantiana is very diverse (49 species), few were regular visitors and likely to act as pollinators. Seventy-four percent of visitor species accounted for only 11% of total visitor abundance and 69% were collected in three or fewer plant populations (of ten). Of the few reliable visitors, Clarkia pollen specialist bees were the most frequent visitors, carried more Clarkia pollen compared to generalist foragers, and were less likely to harbor foreign pollen. Overall, the core group of pollinators was obscured by high numbers of incidental visitors that are unlikely to contribute to pollination. In a geographic context, the composition of specialist pollinator assemblages varied considerably along the abiotic gradient spanning the subspecies’ range. However, the overall abundance of specialist pollinators in plant populations was not influenced by the broad-scale abiotic gradient but strongly affected by local plant community associations. C. x. xantiana populations sympatric with pollinator-sharing congeners were visited twice as often by specialists compared to populations occurring alone. These positive indirect interactions among plant species may promote population persistence and species coexistence by enhancing individual reproductive success.

The Geography of Demography: Long-Term Demographic Studies and Species Distribution Models Reveal a Species Border Limited by Adaptation

Potential causes of species’ geographic distribution limits fall into two broad classes: (1) limited adaptation across spatially variable environments and (2) limited opportunities to colonize unoccupied areas. Combining demographic studies, analyses of demographic responses to environmental variation, and species distribution models, we investigated the causes of range limits in a model system, the eastern border of the California annual plant Clarkia xantiana ssp. xantiana. Vital rates of 20 populations varied with growing season temperature and precipitation: fruit number and overwinter survival of 1-year-old seeds declined steeply, while current-year seed germination increased modestly along west-to-east gradients in decreasing temperature, decreasing mean precipitation, and increasing variation in precipitation. Long-term stochastic finite rate of increase, λs, exhibited a fourfold range and varied among geologic surface materials as well as with temperature and precipitation. Growth rate declined significantly toward the eastern border, falling below 1 in three of the five easternmost populations. Distribution models employing demographically important environmental variables predicted low habitat favorability beyond the eastern border. Models that filtered or weighted population presences by λs predicted steeper eastward declines in favorability and assigned greater roles in setting the distribution to among-year variation in precipitation and to geologic surface material. These analyses reveal a species border likely set by limited adaptation to declining environmental quality.

Reduced pollinator service and elevated pollen limitation at the geographic range limit of an annual plant

Mutualisms are well known to influence individual fitness and the population dynamics of partner species, but little is known about whether they influence species distributions and the location of geographic range limits. Here, we examine the contribution of plant-pollinator interactions to the geographic range limit of the California endemic plant Clarkia xantiana ssp. xantiana. We show that pollinator availability declined from the center to the margin of the geographic range consistently across four years of study. This decline in pollinator availability was caused to a greater extent by variation in the abundance of generalist rather than specialist bee pollinators. Climate data suggest that patterns of precipitation in the current and previous year drove variation in bee abundance because of its effects on cues for bee emergence in the current year and the abundance of floral resources in the previous year. Experimental floral manipulations showed that marginal populations had greater outcross pollen limitation of reproduction, in parallel with the decline in pollinator abundance. Although plants are self-compatible, we found no evidence that autonomous selfing contributes to reproduction, and thus no evidence that it alleviates outcross pollen limitation in marginal populations. Furthermore, we found no association between the distance to the range edge and selfing rate, as estimated from sequence and microsatellite variation, indicating that the mating system has not evolved in response to the pollination environment at the range periphery. Overall, our results suggest that dependence on pollinators for reproduction may be an important constraint limiting range expansion in this system.

Correlations among Fertility Components Can Maintain Mixed Mating in Plants

Classical models studying the evolution of self‐fertilization in plants conclude that only complete selfing and complete outcrossing are evolutionarily stable. In contrast with this prediction, 42% of seed‐plant species are reported to have rates of self‐fertilization between 0.2 and 0.8. We propose that many previous models fail to predict intermediate selfing rates because they do not allow for functional relationships among three components of reproductive fitness: self‐fertilized ovules, outcrossed ovules, and ovules sired by successful pollen export. Because the optimal design for fertility components may differ, conflicts among the alternative pathways to fitness are possible, and the greatest fertility may be achieved with some self‐fertilization. Here we develop and analyze a model to predict optimal selfing rates that includes a range of possible relationships among the three components of reproductive fitness, as well as the effects of evolving inbreeding depression caused by deleterious mutations and of selection on total seed number. We demonstrate that intermediate selfing is optimal for a wide variety of relationships among fitness components and that inbreeding depression is not a good predictor of selfing‐rate evolution. Functional relationships subsume the myriad effects of individual plant traits and thus offer a more general and simpler perspective on mating system evolution.

Population Structure and Its Effects on Patterns of Nucleotide Polymorphism in Teosinte (Zea mays ssp. parviglumis)

Surveys of nucleotide diversity in the wild ancestor of maize, Zea mays ssp. parviglumis, have revealed genomewide departures from the standard neutral equilibrium (NE) model. Here we investigate the degree to which population structure may account for the excess of rare polymorphisms frequently observed in species-wide samples. On the basis of sequence data from five nuclear and two chloroplast loci, we found significant population genetic structure among seven subpopulations from two geographic regions. Comparisons of estimates of population genetic parameters from species-wide samples and subpopulation-specific samples showed that population genetic subdivision influenced observed patterns of nucleotide polymorphism. In particular, Tajimas D was significantly higher (closer to zero) in subpopulation-specific samples relative to species-wide samples, and therefore more closely corresponded to NE expectations. In spite of these overall patterns, the extent to which levels and patterns of polymorphism within subpopulations differed from species-wide samples and NE expectations depended strongly on the geographic region (Jalisco vs. Balsas) from which subpopulations were sampled. This may be due to the demographic history of subpopulations in those regions. Overall, these results suggest that explicitly accounting for population structure may be important for studies examining the genetic basis of ecologically and agronomically important traits as well as for identifying loci that have been the targets of selection.