Ryan D. Briscoe Runquist

Asymmetric and frequency‐dependent pollinator‐mediated interactions may influence competitive displacement in two vernal pool plants

A plant species immigrating into a community may experience a rarity disadvantage due to competition for the services of pollinators. These negative reproductive interactions have the potential to lead to competitive displacement or exclusion of a species from a site. In this study, we used one- and two-species arrays of potted plants to test for density and frequency dependence in pollinator-mediated and above-ground intraspecific and interspecific competition between two species of Limnanthes that have overlapping ranges, but rarely occur in close sympatry. There were asymmetric competitive effects; the species responded differently to their frequency within 16-plant replacement series arrays. Limnanthes douglasii rosea experienced stronger reductions in lifetime and per-flower fertility, likely due to pollinator-mediated competition with Limnanthes alba. This effect may be linked to asymmetrical competition through heterospecific pollen transfer. This study demonstrates that pollinator-mediated competition may discourage establishment of L. d. rosea in sites already occupied by its congener.

Rapid evolution of reproductive isolation between incipient outcrossing and selfing Clarkia species

A major goal of speciation research is to understand the processes involved in the earliest stages of the evolution of reproductive isolation (RI). One important challenge has been to identify systems where lineages have very recently diverged and opportunities for hybridization are present. We conducted a comprehensive examination of the components of RI across the life cycle of two subspecies of Clarkia xantiana, which diverged recently (ca. 65,000 bp). One subspecies is primarily outcrossing, but self‐compatible, whereas the other is primarily selfing. The subspecies co‐occur in a zone of sympatry but hybrids are rarely observed. Premating barriers resulted in nearly complete isolation in both subspecies with flowering time and pollinator preference (for the outcrosser over the selfer) as the strongest barriers. We found that the outcrosser had consistently more competitive pollen, facilitating hybridization in one direction, but no evidence for pollen–pistil interactions as an isolating barrier. Surprisingly, postzygotic isolation was detected at the stage of hybrid seed development, but in no subsequent life stages. This crossing barrier was asymmetric with crosses from the selfer to outcrosser most frequently failing. Collectively, the results provide evidence for rapid evolution of multiple premating and postzygotic barriers despite a very recent divergence time.

Pollinator-mediated competition between two congeners, Limnanthes douglasii subsp. rosea and L. alba (Limnanthaceae)

PREMISE OF STUDY Pollinator visits are essential for reproduction in many plants, yet interspecific movements of pollinators can also lead to competitive interactions between coflowering species. Pollination-mediated reductions in fertility could potentially lead to exclusion of competing plant species, and may generate spatial variation in the associations among coflowering species across a landscape. METHODS I documented the potential for heterospecific pollen transfer to cause competitive interactions between two annual grassland species native to California, Limnanthes douglasii subsp. rosea and L. alba, two reproductively incompatible species that have broadly overlapping geographic ranges in the foothills of the Sierra Nevada. I observed pollinator movement in constructed arrays and controlled crosses in the greenhouse and field to investigate the consequences of heterospecific pollen transfer. KEY RESULTS Pollinators move readily between species when they are presented together in experimental arrays. In the greenhouse, deposition of heterospecific pollen decreased fertility in both species. The decrease in seeds produced per flower was much more pronounced in L. d. rosea (90.6% reduction) than in L. alba (40.8% reduction). In field experiments, L. d. rosea plants that received pollen from heterospecific neighbors first showed >50% reduction in per-flower fertility. CONCLUSIONS Under natural pollination conditions, heterospecific pollen transfer has the ability to decrease the fertility of L. d. rosea when it occurs at low frequency in mixed stands. Accordingly, pollinator-mediated competition may contribute to the locally disjunct distributions of these two species. It may also influence important restoration decisions in vernal pool habitats.

Global biogeography of mating system variation in seed plants.

Latitudinal gradients in biotic interactions have been suggested as causes of global patterns of biodiversity and phenotypic variation. Plant biologists have long speculated that outcrossing mating systems are more common at low than high latitudes owing to a greater predictability of plant-pollinator interactions in the tropics; however, these ideas have not previously been tested. Here, we present the first global biogeographic analysis of plant mating systems based on 624 published studies from 492 taxa. We found a weak decline in outcrossing rate towards higher latitudes and among some biomes, but no biogeographic patterns in the frequency of self-incompatibility. Incorporating life history and growth form into biogeographic analyses reduced or eliminated the importance of latitude and biome in predicting outcrossing or self-incompatibility. Our results suggest that biogeographic patterns in mating system are more likely a reflection of the frequency of life forms across latitudes rather than the strength of plant-pollinator interactions.

Resource reallocation does not influence estimates of pollen limitation or reproductive assurance in Clarkia xantiana subsp. parviflora (Onagraceae)

UNLABELLED PREMISE OF STUDY Studies of pollen limitation and the reproductive assurance value of selfing are important for examining the process of floral and mating system evolution in flowering plants. Recent meta-analyses have shown that common methods for measuring pollen limitation may often lead to biased estimates. Specifically, experiments involving single- or few-flower manipulations per plant tend to overestimate pollen limitation compared to those involving manipulations on most or all flowers per plant. Little previous work has explicitly tested for reallocation within individual systems using alternative methods and response variables. • METHODS We performed single-flower and whole-plant pollen supplementation and emasculation of flowers of Clarkia xantiana subsp. parviflora to estimate pollen limitation (PL) and reproductive assurance (RA). We compared levels of PL and RA using the following response variables: fruit set, seeds/flower, and seeds/plant. We also assessed the germination and viability of seeds to evaluate potential variation in pollen quality among treatments. • KEY RESULTS Autonomous selfing in Clarkia xantiana subsp. parviflora eliminates pollen limitation and provides reproductive assurance. Estimates from single-flower manipulations were not biased, closely resembling those from whole-plant manipulations. All three response variables followed the same pattern, but treatments were only significantly different for seeds/flower. Pollen quality, as indicated by seed viability, did not differ among treatments. • CONCLUSIONS Partial plant manipulations provided reliable estimates of pollen limitation and reproductive assurance. These estimates were also unaffected by accounting for pollen quality. Although whole plant manipulations are desirable, this experiment demonstrates that in some systems partial plant manipulations can be used in studies where whole-plant manipulations are not feasible.

No association between plant mating system and geographic range overlap

PREMISE OF THE STUDY Automatic self-fertilization may influence the geography of speciation, promote reproductive isolation between incipient species, and lead to ecological differentiation. As such, selfing taxa are predicted to co-occur more often with their closest relatives than are outcrossing taxa. Despite suggestions that this pattern may be general, the extent to which mating system influences range overlap in close relatives has not been tested formally across a diverse group of plant species pairs. METHODS We tested for a difference in range overlap between species pairs for which zero, one, or both species are selfers, using data from 98 sister species pairs in 20 genera across 15 flowering plant families. We also used divergence time estimates from time-calibrated phylogenies to ask how range overlap changes with divergence time and whether this effect depends on mating system. KEY RESULTS We found no evidence that automatic self-fertilization influenced range overlap of closely related plant species. Sister pairs with more recent divergence times had modestly greater range overlap, but this effect did not depend on mating system. CONCLUSIONS The absence of a strong influence of mating system on range overlap suggests that mating system plays a minor or inconsistent role compared with many other mechanisms potentially influencing the co-occurrence of close relatives.

Mating System Evolution under Strong Pollen Limitation: Evidence of Disruptive Selection through Male and Female Fitness in Clarkia xantiana

Selection on floral traits in hermaphroditic plants is determined by both male and female reproductive success. However, predictions regarding floral trait and mating system evolution are often based solely on female fitness. Selection via male fitness has the potential to affect the outcomes of floral evolution. In this study, we used paternity analysis to assess individual selfing rates and selection on floral traits via male and female fitness in an experimental population of Clarkia xantiana where pollen limitation of seed set was strong. We detected selection through both female and male fitness with reinforcing or noninterfering patterns of selection through the two sex functions. For female fitness, selection favored reduced herkogamy and protandry, traits that promote increased autonomous selfing. For male fitness, selection on petal area was disruptive, with higher trait values conferring greater pollinator attraction and outcross siring success and smaller trait values leading to higher selfed siring success. Combining both female and male fitness, selection on petal area and protandry was disruptive because intermediate phenotypes were less successful as both males and females. Finally, functional relationships among male and female fertility components indicated that selfing resulted in seed discounting and pollen discounting. Under these functional relationships, the evolutionarily stable selfing rate can be intermediate or predominantly selfing or outcrossing, depending on the segregating load of deleterious mutations.

Mating system divergence affects the distribution of sequence diversity within and among populations of recently diverged subspecies of Clarkia xantiana (Onagraceae).

PREMISE OF THE STUDY The population biology of outcrossing and self-fertilizing taxa is thought to differ because of the advantage that selfers have in colonizing unoccupied sites where mates and pollinators may be limiting (Bakers Law). This reduced tendency for outcrossers to colonize new sites, along with their greater dependence on pollinators to disperse pollen, has the potential to differently influence the genetic diversity and structure of outcrossing and selfing populations. METHODS We conducted a comparative population genetic study of two sister outcrossing and selfing subspecies of Clarkia xantiana that have very recently diverged. We used DNA sequence variation (>40 kb from eight nuclear loci) from large samples of individuals from 14 populations to assess geographic patterns of genetic diversity and make inferences about the demographic and colonization histories of each subspecies. KEY RESULTS We show that sequence variation is strongly reduced across all selfing populations. The demographic history of selfing populations exhibits recent colonization bottlenecks, whereas such bottlenecks are rarely observed for the outcrosser. The greater effect of genetic drift in the selfer has resulted in strong population genetic structure, but with no pattern of isolation by distance. By contrast, the stronger effect of gene flow in the outcrosser has resulted in considerably less structure, but a significant pattern of isolation by distance. CONCLUSIONS Taken together, our results suggest that selfing populations are not at migration-drift equilibrium, are affected by strong episodes of genetic drift during colonization, and experience little or no subsequent gene flow from other populations after those founder events.

Community Phenology and Its Consequences for Plant-Pollinator Interactions and Pollen Limitation in a Vernal Pool Plant

Premise of research. Pollen limitation may affect the potential for plants to set a full complement of seeds, persist in a community, and influence floral evolution. The level of pollen limitation experienced by a population may be influenced by the phenology of the pollinator and coflowering plant community. Methodology. In this study, I used pollen supplementation to test for pollen limitation throughout a season in a population of insect-pollinated, vernal pool annuals, Limnanthes douglasii rosea. I collected information on the phenological changes in pollinator-sharing, coflowering community members and pollinator community composition in three flowering seasons to investigate the potential impacts of community composition on pollen limitation. Last, I investigated components of pollen transfer that may impact pollen limitation: pollen loads found on pollinator bodies and pollen found on stigmatic surfaces after visitation. Pivotal results. I found that L. d. rosea experiences significant pollen limitation during the early season when evaluated over the entire flowering season and that the level of pollen limitation is related to changes in the coflowering community and changes in the pollinator community. The effects of coflowering community and pollinator community composition are also correlated with seasonality. Both components of pollen transfer are positively associated with greater abundances of L. d. rosea and coflowering community member Lasthenia spp. Conclusions. This study demonstrates that pollen limitation can change throughout a season and that pollen limitation and factors that affect the extent of pollen limitation are influenced by community context.