Åsa Lankinen

How does breeding system variation modulate sexual antagonism

The study of sexually antagonistic (SA) traits remains largely limited to dioecious (separate sex), mobile animals. However, the occurrence of sexual conflict is restricted neither by breeding system (the mode of sexual reproduction, e.g. dioecy or hermaphroditism) nor by sessility. Here, we synthesize how variation in breeding system can affect the evolution and expression of intra- and inter-locus sexual conflicts in plants and animals. We predict that, in hermaphrodites, SA traits will (i) display lower levels of polymorphism; (ii) respond more quickly to selection; and (iii) involve unique forms of interlocus conflict over sex allocation, mating roles and selfing rates. Explicit modelling and empirical tests in a broader range of breeding systems are necessary to obtain a general understanding of the evolution of SA traits.

Delayed stigma receptivity in Collinsia heterophylla (Plantaginaceae): Genetic variation and adaptive significance in relation to pollen competition, delayed self-pollination and mating-system evolution

To increase our knowledge about mating-system evolution, we need to understand the relationship between specific floral traits and mating system. Species of Collinsia (Plantaginaceae) vary extensively in mating system; this variation is associated with variation in floral morphology and development and with the timing of self-pollination. Counterintuitively, large-flowered, more outcrossing species tend to have delayed stigma receptivity, reducing the amount of time that the stigma is receptive to cross-pollination before autonomous self-pollination. To understand how the timing of stigma receptivity is related to mating-system evolution, we studied in detail the timing of both stigma receptivity and self-pollination (anther-stigma contact) in two greenhouse-grown populations of large-flowered Collinsia heterophylla. Crosses on emasculated flowers at different stages of floral development always produced seeds, suggesting that cross-fertilization can be effected by pollen arriving prior to physiological receptivity. Phenotypic and genetic variation within populations in the timing of stigma receptivity and anther-stigma contact was substantial, although slightly less for the contact. Despite strong interspecific and interpopulation correlations, we did not find an among-genet phenotypic correlation between the traits. This indicates that each trait may respond independently to selection, and the trait association may be the result of correlational selection.

Pollen donor identity affects timing of stigma receptivity in Collinsia heterophylla (Plantaginaceae): a sexual conflict during pollen competition?

Theory predicts that, during pollen competition, selection may favor a pollen trait that increases donor competitive ability at the expense of the female reproductive function. One such pollen trait could be manipulation of the onset of stigma receptivity. We evaluated the potential occurrence of this kind of sexual conflict by testing female control of the timing of stigma receptivity in the self‐compatible annual Collinsia heterophylla. By performing one‐donor crosses in the greenhouse, we found that differences in both recipients and pollen donors influenced when stigmas became receptive. Because we did not detect an interaction effect, our result suggests that some donors were consistently better than others at germinating pollen and siring seeds earlier. Unexpectedly, self‐pollen was able to fertilize seeds earlier during floral development compared with outcross pollen. These results suggest that female control on timing of stigma receptivity is not complete in this species. In addition, fertilizations that occurred early during floral development resulted in fewer seeds than later fertilizations, possibly indicating a cost of lost control over the onset of receptivity. The ability of pollen donors to influence the timing of stigma receptivity might reflect a conflict between the sexual functions in C. heterophylla.

SEXUAL CONFLICT OVER FLORAL RECEPTIVITY

Abstract In flowering plants, the onset and duration of female receptivity vary among species. In several species the receptive structures wilt upon pollination. Here we explore the hypothesis that postpollination wilting may be influenced by pollen and serve as a general means to secure paternity of the pollen donor at the expense of female fitness. Taking a game-theoretical approach, we examine the potential for the evolution of a pollen-borne wilting substance, and for the coevolution of a defense strategy by the recipient plant. The model without defense predicts an evolutionarily stable strategy (ESS) for the production of wilting substance. The ESS value is highest when pollinator visiting rates are intermediate and when the probability that pollen from several donors arrives at the same time is low. This finding has general implications in that it shows that male traits to secure paternity also can evolve in species, such as plants, where mating is not strictly sequential. We further model coevolution of the wilting substance with the timing of stigma receptivity. We assume that pollen-receiving plants can reduce the costs induced by toxic pollen by delaying the onset of stigmatic receptivity. The model predicts a joint ESS, but no female counter-adaptation when the wilting substance is highly toxic. This indicates that toxicity affects the probability that a male manipulative trait stays beneficial (i.e., not countered by female defense) over evolutionary time. We discuss parallels to male induced changes in female receptivity known to occur in animals and the role of harm for the evolution of male manipulative adaptations.

Pollen-tube growth rates in Collinsia heterophylla (Plantaginaceae): one-donor crosses reveal heritability but no effect on sporophytic-offspring fitness.

BACKGROUND AND AIMS Evolutionary change in response to natural selection will occur only if a trait confers a selective advantage and there is heritable variation. Positive connections between pollen traits and fitness have been found, but few studies of heritability have been conducted, and they have yielded conflicting results. To understand better the evolutionary significance of pollen competition and its potential role in sexual selection, the heritability of pollen tube-growth rate and the relationship between this trait and sporophytic offspring fitness were investigated in Collinsia heterophylla. METHODS Because the question being asked was if female function benefited from obtaining genetically superior fathers by enhancing pollen competition, one-donor (per flower) crosses were used in order to exclude confounding effects of post-fertilization competition/allocation caused by multiple paternity. Each recipient plant was crossed with an average of five pollen donors. Pollen-tube growth rate and sporophytic traits were measured in both generations. KEY RESULTS Pollen-tube growth rate in vitro differed among donors, and the differences were correlated with in vivo growth rate averaged over two to four maternal plants. Pollen-tube growth rate showed significant narrow-sense heritability and evolvability in a father-offspring regression. However, this pollen trait did not correlate significantly with sporophytic-offspring fitness. CONCLUSIONS These results suggest that pollen-tube growth rate can respond to selection via male function. The data presented here do not provide any support for the hypothesis that intense pollen competition enhances maternal plant fitness through increased paternity by higher-quality sporophytic fathers, although this advantage cannot be ruled out. These data are, however, consistent with the hypothesis that pollen competition is itself selectively advantageous, through both male and female function, by reducing the genetic load among successful gametophytic fathers (pollen), and reducing inbreeding depression associated with self-pollination in plants with mix-mating systems.

Pollen competition reduces inbreeding depression in Collinsia heterophylla (Plantaginaceae)

We tested two predictions of the hypothesis that competition between self‐pollen may mitigate negative genetic effects of inbreeding in plants: (1) intense competition among self‐pollen increases offspring fitness; and (2) pollen competition reduces the measured strength of inbreeding depression. We used Collinsia heterophylla (Plantaginaceae), an annual with a mixed mating system, to perform controlled crosses in which we varied both the size of the pollen load and the source of pollen (self vs. outcross). Fitness of selfed offspring was higher in the high pollen‐load treatment. Our second prediction was also upheld: inbreeding depression was, on average, lower when large pollen loads were applied (11%) relative to the low pollen‐load treatment (28%). The reduction was significant for two fitness components relatively late in the life‐cycle: number of surviving seedlings and pollen‐tube growth rate in vitro. These findings suggest that intermittent inbreeding, which leads to self‐fertilization in plants with genetic loads, may select for traits that enhance pollen competition.

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.

Conflicting selection pressures on reproductive functions and speciation in plants.

Recent developments in the field of genetic divergence and speciation focus more on diversifying processes than on geographic mode of speciation (i.e. allopatric versus sympatric). Some of these new theories concern speciation driven by conflicts between the sexes. Even though it is well known that the two reproductive functions in plants can have different selective optima, sexual selection in plants is by many assumed to be weak or non-existent. Here we outline potential sexual conflicts in plants and discuss how selection pressures generated by such conflicts may influence genetic divergence. There is opportunity for conflicting selection pressures between individuals, such as manipulative pollen traits that enhance male reproductive success at the expense of the female reproductive function. Within individual plants, fitness of the male function (pollen export) and fitness of the female function (pollen import) may be optimised by different traits, leading to conflicting selection pressures in relation to pollen transfer. This may affect selection for floral specialisation versus floral generalisation in animal-pollinated species. We believe that selection pressures generated by sexual conflict need to be appreciated in order to fully understand microevolutionary processes which may lead to genetic divergence and speciation in plants.

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.

Effects of Soil pH and Phosphorus on In Vitro Pollen Competitive Ability and Sporophytic Traits in Clones of Viola tricolor

Greenhouse‐grown clones of Viola tricolor were used to evaluate the importance of genetic effects on in vitro pollen tube growth rate in relation to the influence of two environmental soil factors—pH and phosphorus content. After 1 mo in different soil treatments, individual pollen tube growth rate was affected by a genotype by phosphorus interaction, while it was unaffected by either main effects. Though individuals differed in their response to phosphorus availability, the rank order of pollen donors remained consistent between treatments; i.e., the pollen donors with the highest pollen tube growth rate were the same in all soil conditions. Sporophytic traits were also affected by a genotype by phosphorus interaction. The response of pollen growth and sporophytic traits to soil phosphorus content were correlated within individuals in the high pH treatments. These results, in combination with a high value of clonal repeatability of pollen tube growth rate, indicate that pollen competitive ability has a genetic basis in this species. One prerequisite for this trait to have evolutionary effects on male fitness is thus fulfilled. Furthermore, if the response to phosphorus among pollen donors is more pronounced under natural conditions, variation in this environmental factor within populations has the potential to maintain some genetic variation in pollen tube growth rate even if this trait is constantly selected.