Josefin A. Madjidian

Displacement of a native by an alien bumblebee: lower pollinator efficiency overcome by overwhelmingly higher visitation frequency

Biological invasions might constitute a major threat to mutualisms. Introduced pollinators might competitively displace their native counterparts, which in turn affects the pollination of native plants, if native and alien visitors differ in pollinator effectiveness. Since its invasion in 1994 into south-west Argentina, the introduced European bumblebee Bombus ruderatus has continuously increased in abundance, along with a simultaneous decrease in the abundance of the native Bombus dahlbomii. The latter is the only native bumblebee species of the temperate forests of southern South America, and the main pollinator of the endemic herb Alstroemeria aurea. In order to evaluate the impact of the ongoing displacement of the native by the alien bumblebee, we compared the pollinator effectiveness (i.e., the combination of pollinator efficiency per visit and visitation frequency) between both bumblebee species, as well as related pollinator traits that might account for potential differences in pollinator efficiency. Native Bombus dahlbomii, which has a larger body and spent more time per flower, was the more efficient pollinator compared to Bombus ruderatus, both in terms of quantity and quality of pollen deposited per visit. However, Bombus ruderatus was a much more frequent flower visitor than Bombus dahlbomii. As a consequence, Bombus ruderatus is nowadays a more effective pollinator of A. aurea than its native congener. Despite the lack of evidence of an increase in seed set at the population level, comparisons with historical records of Bombus dahlbomii abundances prior to Bombus ruderatus’ invasion suggest that the overall pollination intensity of A. aurea might in fact have risen as a consequence of this invasion. Field experiments like these, that incorporate the natural variation in abundance of native and alien species, are powerful means to demonstrate that the consequences of invasions are more complex than previous manipulated and controlled experiments have suggested.

Enhancing pollen competition by delaying stigma receptivity: Pollen deposition schedules affect siring ability, paternal diversity, and seed production in Collinsia heterophylla (Plantaginaceae)

PREMISE OF THE STUDY Even though pollen deposition schedules may have profound effects on the evolutionary outcome of pollen competition, few studies have investigated such effects in relation to pistil traits such as delayed stigma receptivity that enhance pollen competition. In Collinsia heterophylla, a largely outcrossing species with delayed stigma receptivity, we performed a series of controlled crosses involving several donors to understand how timing of pollen deposition influences siring ability, paternal diversity, and offspring fitness. METHODS Pollen was applied to fully receptive stigmas either as mixtures or consecutively with or without a time lag to mimic cases with early or delayed stigma receptivity. We used a genetic marker to assess offspring paternity. KEY RESULTS As expected, siring ability was affected by application order in crosses without a time lag, providing a first-donor advantage for pollen arriving on unreceptive stigmas. However, because pollen donor identity influenced siring ability, delaying stigma receptivity may still favor pollen of high competitive ability. In crosses on fully receptive pistils with a time lag of 24 h, a surprisingly high proportion of seeds (12-47%) were sired by pollen applied last. A novel finding was that pollen applied only once (as a mixture), mimicking delayed stigma receptivity, led to higher paternal diversity within progeny families, which was associated with increased seed production. CONCLUSIONS Our results suggest fitness advantages of enhancing pollen competition by delaying stigma receptivity in C. heterophylla, particularly in relation to increased paternal diversity.

Active males, reactive females: stereotypic sex roles in sexual conflict research?

Sexual selection research has always been a subject for debate. Much of the criticism has concerned the imposition of conventional sex roles based on an anthropomorphic view of animals imposed by the researcher. This conventional view may have hampered research, for example from acknowledging male mate choice. Sexual conflict theory is a fast-growing research field, which initially stems from sexual selection research. We investigated how the sexes are described in sexual conflict research and what characteristics they are assigned. We assessed these topics with literature studies of (1) the terminology used and (2) what parameters are incorporated in sexual conflict models. We found that males and females are consequently described with different words, which have different connotations regarding activity in the conflict. Furthermore, theoretical models mainly investigate conflict costs for females, although costs for both sexes are necessary for coevolutionary dynamics. We argue that sexual conflict research uses stereotypic characterizations of the sexes, where males are active and females reactive. Thus, previous discussions on the use of anthropomorphic terms in sexual selection seem not to have had any impact on sexual conflict research, which is why the topic of stereotyping the sexes is still of current importance. We suggest that scientific gains can be made by eliminating a sex-stereotyped perspective.

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.

Selection on pollen and pistil traits during pollen competition is affected by both sexual conflict and mixed mating in a self-compatible herb

PREMISE OF THE STUDY Although much attention has focused on the diversity of plant mating systems, only a few studies have considered the joint effects of mating system and sexual conflict in plant evolution. In mixed-mating Collinsia heterophylla, a sexual conflict over timing of stigma receptivity is proposed: pollen with a capacity to induce early onset of stigma receptivity secures paternity for early-arriving pollen (at the expense of reduced maternal seed set), whereas late onset of stigma receptivity mitigates the negative effects of early-arriving pollen. Here we investigated whether selection on pollen and pistil traits involved in sexual conflict is affected by the presence of both outcross- and self-pollen (mixed mating) during pollen competition. METHODS We conducted two-donor crosses at different floral developmental stages to explore male fitness (siring ability) and female fitness (seed set) in relation to male and female identity, pollen and pistil traits, and type of competitor pollen (outcross vs. self). KEY RESULTS Late-fertilizing pollen rather than rapidly growing pollen tubes was most successful in terms of siring success, especially in competition with self-pollen after pollination at early floral stages. Late stigma receptivity increased seed set after early-stage pollinations, in agreement with selection against antagonistic pollen. CONCLUSIONS Selection on pollen and pistil traits in C. heterophylla is affected by both sexual conflict and mixed mating, suggesting the importance of jointly considering these factors in plant evolution.

Influence of number of pollinations and pollen load size on maternal fitness costs in Collinsia heterophylla: implications for existence of a sexual conflict over timing of stigma receptivity.

Costs related to pollen competition have rarely been considered, but are expected in the case of sexual conflict where male and female sexual functions have opposing evolutionary interests. In Collinsia heterophylla, delayed stigma receptivity is beneficial as it enhances pollen competition. A sexual conflict over timing of stigma receptivity has been proposed in this species as early pollination, following one‐time pollinations, is advantageous to pollen donors at a cost of reduced maternal seed set (measured as seed number). In this study, we explored whether the maternal cost was still present following an additional pollination. We hypothesized that the cost is caused either by harm related to early pollen presence or by factors unrelated to harm. We performed pollinations at different stages of floral development, either one or two pollinations (24‐h time lag), and varied the size of the first pollen load in the latter category. Early pollination reduced seed biomass also after two‐time pollinations, suggesting a persistent maternal cost of early pollen presence. Further, pollen load size modified seed production, possibly indicating that dose‐dependent harm influences the maternal cost of early fertilization. Our results strongly suggest negative effects of pollen competition on maternal fitness following early pollination, which is consistent with the existence of a sexual conflict over timing of stigma receptivity. In conclusion, we propose that much could be gained if more plant studies considered the potential for fitness costs in relation to sexual conflict, particularly those investigating pollen–pistil interactions.

Estimation of heritability, evolvability and genetic correlations of two pollen and pistil traits involved in a sexual conflict over timing of stigma receptivity in Collinsia heterophylla (Plantaginaceae).

BACKGROUND AND AIMS Heritable genetic variation is crucial for selection to operate, yet there is a paucity of studies quantifying such variation in interactive male/female sexual traits, especially those of plants. Previous work on the annual plant Collinsia heterophylla, a mixed-mating species, suggests that delayed stigma receptivity is involved in a sexual conflict: pollen from certain donors fertilize ovules earlier than others at the expense of reduced maternal seed set and lower levels of pollen competition. METHODS Parent-offspring regressions and sib analyses were performed to test for heritable genetic variation and co-variation in male and female interactive traits related to the sexual conflict. KEY RESULTS SOME heritable variation and evolvability were found for the female trait (delayed stigma receptivity in presence of pollen), but no evidence was found for genetic variation in the male trait (ability to fertilize ovules early). The results further indicated a marginally significant correlation between a males ability to fertilize early and early stigma receptivity in offspring. However, despite potential indirect selection of these traits, antagonistic co-evolution may not occur given the lack of heritability of the male trait. CONCLUSIONS To our knowledge, this is the first study of a plant or any hermaphrodite that examines patterns of genetic correlation between two interactive sexual traits, and also the first to assess heritabilities of plant traits putatively involved in a sexual conflict. It is concluded that the ability to delay fertilization in presence of pollen can respond to selection, while the pollen trait has lower evolutionary potential.

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 (i) delayed stigma receptivity, which intensifies pollen competition, and (ii) early fertilization forced by pollen, which reduces seed set. We investigated the potential for the conflict to occur under field conditions and performed glasshouse 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 glasshouse, 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 the 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.

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.

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.