Floral scent and pollinator visitation in relation to floral colour morph in the mixed-mating annual herb Collinsia heterophylla

Even though floral scent is of major importance for pollinator attraction, it is less investigated than other floral traits. Previous studies suggest the importance of joint exploration of olfactory and visual floral cues to understand plant-pollinator interactions. We investigated flower scents in Collinsia heterophylla, a bee-pollinated, annual herb a with mixed-mating system combining self- and outcross-pollination. In Collinsia, floral size and development variation is related to mating system, ranging from large-flowered mixed-mating species to small-flowered self-pollinated species. However, to our knowledge, flower scent has not been described in any species in the genus. We also studied whether flower-emitted volatiles were coupled to presence versus absence of a coloured band on the upper lip within a population in C. heterophylla, and if these colour morphs affected pollinator visitation. We performed headspace collections of volatiles in the greenhouse from potted flowering plants, and compared these to controls in the bud stage. Flower-specific volatiles were highly dominated by terpenoid compounds typical of bee-pollinated plants, such as beta-myrcene, (Z)- and (E)-ocimene and sesquiterpenes (E)-alpha-bergamotene and beta-sesquiphellandrene. The aliphatic ester methyl hexanoate was also prominent, together with additional esters, whereas methyl cinnamate constituted the only aromatic compound. Floral colour morphs showed no qualitative difference in volatiles, but the coloured morph produced significantly higher quantities for seven of the 26 individual flower compounds. A field experiment performed within a natural population, using behavioural observations and florescent dyes dusted on the flowers, could not detect any differences in pollinator visitation between colour morphs. We conclude that C. heterophylla flowers emit volatile compounds commonly associated with attraction of their most important pollinators. It would be highly interesting to explore the function of floral scent for pollinator attraction and relate floral scent to mating system variation across Collinsia for a better understanding of pollinator influence on floral evolution

Sexual Conflict and Sexually Antagonistic Coevolution in an Annual Plant

BACKGROUND: Sexual conflict theory predicts sexually antagonistic coevolution of reproductive traits driven by conflicting evolutionary interests of two reproducing individuals. Most studies of the evolutionary consequences of sexual conflicts have, however, to date collectively investigated only a few species. In this study we used the annual herb Collinsia heterophylla to experimentally test the existence and evolutionary consequences of a potential sexual conflict over onset of stigma receptivity. METHODOLOGY/PRINCIPAL FINDINGS: We conducted crosses within and between four greenhouse-grown populations originating from two regions. Our experimental setup allowed us to investigate male-female interactions at three levels of geographic distances between interacting individuals. Both recipient and pollen donor identity affected onset of stigma receptivity within populations, confirming previous results that some pollen donors can induce stigma receptivity. We also found that donors were generally better at inducing stigma receptivity following pollen deposition on stigmas of recipients from another population than their own, especially within a region. On the other hand, we found that donors did worse at inducing stigma receptivity in crosses between regions. Interestingly, recipient costs in terms of lowered seed number after early fertilisation followed the same pattern: the cost was apparent only if the pollen donor belonged to the same region as the recipient. CONCLUSION/SIGNIFICANCE: Our results indicate that recipients are released from the cost of interacting with local pollen donors when crossed with donors from a more distant location, a pattern consistent with a history of sexually antagonistic coevolution within populations. Accordingly, sexual conflicts may have important evolutionary consequences also in plants

Effect of root contact on pollen competitive ability in a hermaphroditic winter-annual herb

Presence of a root neighbor can induce changes in root allocation and pollen traits, but only a limited number of studies have investigated such effects on pollen. To learn more about effects of root contact on pollen competitive ability, we studied plants of the hermaphroditic winter-annual Collinsia heterophylla, native to California. We cultivated plants in two-pot treatments with roots kept either separate or intermingled with the same amount of resources. Pollen-tube growth rate, as an indication of pollen competitive ability, was affected by root treatment but the response varied among competing plant families. The response to root-treatment was not an effect of differential resource uptake of the two competitors. Root biomass was significantly higher when roots were intermingled compared to separate. This finding adds to the number of species with a strategic root response in the presence of competitors, but could also be a consequence of a larger rooting volume. Allocation to pollen performance versus roots in the presence of a competitor was lower in small plants and higher in large plants, potentially implying high costs of producing competitive pollen. We conclude that our study demonstrated that pollen tube growth rate is highly sensitive to the root environment in C. heterophylla

Geographic variation in floral traits is associated with environmental and genetic differences among populations of the mixed mating species Collinsia heterophylla (Plantaginaceae)

Relatively few studies have investigated how geography, environmental factors, and genetics affect floral trait variation. We used mixed-mating Collinsia heterophylla Buist to explore variation in a suite of floral traits related to mating system in populations representing four geographic regions of California, USA, and relate this variation to geography, climatic factors, and local site characteristics. We evaluated the environmental vs. genetic trait variability in the greenhouse. Stage of anther–stigma contact correlated positively with temperature, stage of stigma receptivity was negatively associated with vegetation cover, and flower size differed among populations without any clear relation to environmental factors. Greenhouse data indicated heritability for stage of anther– stigma contact, flower size, and time to flowering, and positive correlations between field and greenhouse for stage of stigma receptivity and flower size; however, stage of anther–stigma contact showed a high degree of environmental influence. Stage of anther–stigma contact covaried positively with stage of stigma receptivity and flower size across maternal families, indicating genetic correlations between traits. In conclusion, phenotypic floral variation within mixed-mating C. heterophylla is mostly determined by a genetic component. Geography, environment, and genetics affect traits differently, suggesting that ecological and evolutionary processes contribute to shaping variability in mating system-related traits

Natural selection acts on floral traits associated with selfing rate among populations of Mixed-Mating collinsia heterophylla (Plantaginaceae)

Premise of research. A major aim in plant research is to understand the micro-and macroevolutionary processes generating the great diversity of mating systems and floral traits found in flowering plants. Using Collinsia heterophylla, a mixed-mating species in a genus with described variation in selfing rate and associated floral traits among species, we investigated (i) intraspecific selfing rate variation in relation to variation in environmental factors and floral traits and (ii) whether selection or genetic drift determine floral trait variation. Methodology. We estimated selfing rate in 21 Californian populations by means of microsatellite markers and investigated its relationship with sampling region, altitude, population ground cover, stage of stigma receptivity, stage of anther-stigma contact (indicating stage of self-pollination), flower size, and start of flowering. Phenotypic floral trait differentiation (PST) for the floral traits was contrasted with neutral genetic differentiation (FST). Pivotal results. The population selfing rate ranged between 0.16 and 0.71 and differed between regions, but it did not correlate with environmental factors. The best predictor of high selfing rate was early stigma receptivity. Stage of anther-stigma contact showed a nonlinear quadratic relation with selfing rate. PST was substantially higher than FST in the four traits, suggesting that variation in mating-related floral traits is shaped by natural selection. Conclusions. The importance of stage of stigma receptivity for predicting selfing rate in C. heterophylla is in line with the pattern found among Collinsia species, potentially indicating that microevolutionary processes in mixed mating influence macroevolutionary processes. The detected effect of natural selection acting on stage of stigma receptivity, in combination with previously detected genetic influence on this trait, gives support to the hypothesis that variability in mating system is adaptive

Data from: Sexual antagonism in the pistil varies among populations of a hermaphroditic mixed-mating plant

Sexual conflicts and their evolutionary outcomes may be influenced by population-specific features such as mating system and ecological context; however, very few studies have investigated the link between sexual conflict and mating system. The self-compatible, mixed-mating hermaphrodite Collinsia heterophylla (Plantaginaceae) is thought to exhibit a sexual conflict over timing of stigma receptivity. This conflict involves 1) delayed stigma receptivity, which intensifies pollen competition, and 2) early fertilization forced by pollen, which reduces seed set. We investigated the potential for the conflict to occur under field conditions and performed greenhouse crosses within eight populations to assess its consistency across populations. Flowers were visited, and produced seeds after pollination, at all developmental stages, suggesting that the conflict can be of significance under natural conditions. In the greenhouse, early pollination imposed costs in all populations. Overall, the timing of first seed set was most strongly affected by the maternal parent, denoting stronger female than male ability to influence onset of stigma receptivity. Crosses also revealed a negative relationship between donor- and recipient-related onset of receptivity within individuals, a novel result hinting at trade-offs in sex-allocation or a history of antagonistic selection. Neither timing of stigma receptivity, timing of first seed set, nor pollen competitive ability covaried with population outcrossing rate. In conclusion, these results indicate that sexually antagonistic selection may be present in varying degrees in different populations of C. heterophylla, but this variation does not appear to be directly related to mating system variation

Data from: Sexual antagonism in the pistil varies among populations of a hermaphroditic mixed-mating plant

Sexual conflicts and their evolutionary outcomes may be influenced by population-specific features such as mating system and ecological context; however, very few studies have investigated the link between sexual conflict and mating system. The self-compatible, mixed-mating hermaphrodite Collinsia heterophylla (Plantaginaceae) is thought to exhibit a sexual conflict over timing of stigma receptivity. This conflict involves 1) delayed stigma receptivity, which intensifies pollen competition, and 2) early fertilization forced by pollen, which reduces seed set. We investigated the potential for the conflict to occur under field conditions and performed greenhouse crosses within eight populations to assess its consistency across populations. Flowers were visited, and produced seeds after pollination, at all developmental stages, suggesting that the conflict can be of significance under natural conditions. In the greenhouse, early pollination imposed costs in all populations. Overall, the timing of first seed set was most strongly affected by the maternal parent, denoting stronger female than male ability to influence onset of stigma receptivity. Crosses also revealed a negative relationship between donor- and recipient-related onset of receptivity within individuals, a novel result hinting at trade-offs in sex-allocation or a history of antagonistic selection. Neither timing of stigma receptivity, timing of first seed set, nor pollen competitive ability covaried with population outcrossing rate. In conclusion, these results indicate that sexually antagonistic selection may be present in varying degrees in different populations of C. heterophylla, but this variation does not appear to be directly related to mating system variation

JEB 12656 Glasshouse data

Raw data from the glasshouse experiments conducted for this study. This contains the majority of the data used for this publication. See the sheet titled "Readme" if you need any clarifications

JEB 12656 Field Data

Collection of raw data from the field experiment conducted for this study