Pollinator-mediated interactions in experimental arrays vary with neighbor identity.

PREMISE OF THE STUDY: Local ecological conditions influence the impact of species interactions on evolution and community structure. We investigated whether pollinator-mediated interactions between coflowering plants vary with plant density, coflowering neighbor identity, and flowering season. METHODS: We conducted a field experiment in which flowering time and floral neighborhood were manipulated in a factorial design. Early- and late-flowering Clarkia unguiculata plants were placed into arrays with C. biloba neighbors, noncongeneric neighbors, additional conspecific plants, or no additional plants as a density control. We compared whole-plant pollen limitation of seed set, pollinator behavior, and pollen deposition among treatments. KEY RESULTS: Interactions mediated by shared pollinators depended on the identity of the neighbor and possibly changed through time, although flowering-season comparisons were compromised by low early-season plant survival. Interactions with conspecific neighbors were likely competitive late in the season. Interactions with C. biloba appeared to involve facilitation or neutral interactions. Interactions with noncongeners were more consistently competitive. The community composition of pollinators varied among treatment combinations. CONCLUSIONS: Pollinator-mediated interactions involved competition and likely facilitation, depending on coflowering neighbor. Experimental manipulation helped to reveal context-dependent variation in indirect biotic interactions.

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.

Stability of pollen-ovule ratios in pollinator-dependent versus autogamous Clarkia sister taxa: testing evolutionary predictions.

It has been proposed that natural selection should favor distinct temporal patterns of sex allocation in selfing vs pollinator-dependent taxa. In autogamous selfers in which pollen receipt is highly reliable, selection should favor genotypes that maintain low and stable pollen to ovule (P : O) ratios throughout flowering. By contrast, in outcrossers the optimum P : O ratio of an individual's flowers will depend on pollinator abundances and mating opportunities, both of which may vary over time. In this case, selection may favor temporal variation among flowers in the P : O ratio. An opposing prediction is that selfing taxa will be developmentally more unstable than outcrossers because of lower homeostasis caused by high homozygosity. We compared temporal changes in the P : O ratio in two pairs of sister taxa in the genus Clarkia. We examined hundreds of glasshouse-raised maternal families representing three wild populations each of the outcrossing, insect-pollinated Clarkia unguiculata, the facultatively autogamous Clarkia exilis and the outcrossing and selfing subspecies of Clarkia xantiana: ssp. xantiana and parviflora, respectively. Temporal change in the P : O ratio was significantly greater in both outcrossers than in their selfing sister taxa, although the proportional changes in the P : O ratio (relative to the first bud produced) did not differ significantly between sister taxa (0.07 < P < 0.10). Our results provide partial support for the hypothesis that the P : O ratio is more stable in selfing than in outcrossing taxa and reject the hypothesis that selfers are less stable.

The joint evolution of mating system, floral traits and life history in Clarkia (Onagraceae): genetic constraints vs. independent evolution.

Genetic correlations caused by pleiotropy or linkage disequilibrium may influence the joint evolution of multiple traits as populations or taxa diverge. The evolutionary transition from outcrossing to selfing has occurred numerous times and is often accompanied by phenotypic and genetic changes in multiple traits such as flower size, pollen-ovule ratio, stigma and anther maturity and the age of reproductive maturity. Determining whether the recurring patterns of multitrait change are because of selection on each trait independently and/or the result of genetic correlations among traits can shed light on the mechanism that accounts for such convergence. Here, we evaluate whether floral traits are genetically correlated with each other and/or with whole-plant traits within- and between-populations and taxa. We report results from a greenhouse study conducted on two pairs of sister taxa with contrasting mating systems: the autogamously selfing Clarkia exilis and its predominantly outcrossing progenitor C. unguiculata and the autogamous Clarkia xantiana ssp. parviflora and its outcrossing progenitor C. xantiana ssp. xantiana. We examined variation within and covariation among maternal families in three populations of each taxon with respect to the age at first flower, the rate of successive flower production and the number of days between bud break and anther dehiscence and stigma receptivity within individual flowers. Based on phenotypic divergence between sister taxa, bivariate regressions, correlations among maternal family means and analysis of covariance (ancova), we did not find unilateral support indicating that genetic constraints govern the joint distribution of floral and whole-plant traits.