Sexual Selection In Plants Research Articles

Darwin's 'mystery of mysteries': the role of sexual selection in plant speciation.

Sexual selection is considered one of the key processes that contribute to the emergence of new species. While the connection between sexual selection and speciation has been supported by comparative studies, the mechanisms that mediate this connection remain unresolved, especially in plants. Similarly, it is not clear how speciation processes within plant populations translate into large-scale speciation dynamics. Here, we review the mechanisms through which sexual selection, pollination, and mate choice unfold and interact, and how they may ultimately produce reproductive isolation in plants. We also overview reproductive strategies that might influence sexual selection in plants and illustrate how functional traits might connect speciation at the population level (population differentiation, evolution of reproductive barriers; i.e. microevolution) with evolution above the species level (macroevolution). We also identify outstanding questions in the field, and suitable data and tools for their resolution. Altogether, this effort motivates further research focused on plants, which might potentially broaden our general understanding of speciation by sexual selection, a major concept in evolutionary biology.

Sexual selection on male but not female function in monoecious and dioecious populations of broadleaf arrowhead (Sagittaria latifolia).

Direct measures of sexual selection in plants are rare and complicated by immobility and modular growth. For plants, instantaneous measures of fitness typically scale with size, but covariances between size and mating success could obscure the detection of sexual selection. We measured the magnitude of sexual selection in a monoecious and a dioecious population of the clonal plant Sagittaria latifolia using Bateman gradients (ßss). These gradients were calculated using parentage analysis and residual regression to account for the effects of shoot and clone size on mating and reproductive success. In both populations, (i) there was greater promiscuity via male function than via female function and (ii) ßss were positive, with significant associations between mating and reproductive success for male but not female function. Moreover, estimated βss were similar for the monoecious and dioecious populations, possibly because non-overlapping female and male sex phases in hermaphroditic S. latifolia reduced the scope for interference between sex functions during mating. This study builds on previous studies of selection on plant mating traits, and of sexual selection under experimental conditions, by showing that sexual selection can operate in natural populations of plants, including populations of hermaphrodites.

Measurement of sexual selection in plants made easier

A recommendation of: Dorken, ME and Perry LE Correlated paternity measures mate monopolization and scales with the magnitude of sexual selection 10.1111/jeb.13013

Pollen--tiny and ephemeral but not forgotten: New ideas on their ecology and evolution.

Ecologists and evolutionary biologists have been interested in the functional biology of pollen since the discovery in the 1800s that pollen grains encompass tiny plants (male gametophytes) that develop and produce sperm cells. After the discovery of double fertilization in flowering plants, botanists in the early 1900s were quick to explore the effects of temperature and maternal nutrients on pollen performance, while evolutionary biologists began studying the nature of haploid selection and pollen competition. A series of technical and theoretic developments have subsequently, but usually separately, expanded our knowledge of the nature of pollen performance and how it evolves. Today, there is a tremendous diversity of interests that touch on pollen performance, ranging from the ecological setting on the stigma, structural and physiological aspects of pollen germination and tube growth, the form of pollen competition and its role in sexual selection in plants, virus transmission, mating system evolution, and inbreeding depression. Given the explosion of technical knowledge of pollen cell biology, computer modeling, and new methods to deal with diversity in a phylogenetic context, we are now more than ever poised for a new era of research that includes complex functional traits that limit or enhance the evolution of these deceptively simple organisms.

Sexual selection in plants

Summary Darwin's theory of evolution by natural selection provided an immediately convincing explanation for the close fit between form and function in nature that had previously only been explicable in terms of supernatural design. Traits evolved in a way that improved their bearer's chances of survival and its success at producing offspring. But what could be said of exaggerated ornamental traits such as the long and lurid tail feathers of many male birds and the ferocious looking mandibles and horned protuberances of various male insects, which were almost certain to compromise their bearer's survival? To explain these traits, Darwin proposed the theory of sexual selection, first in ‘Origin of Species' and then, at greater length, in ‘The Descent of Man'. In a nutshell, he argued that certain traits (secondary sex characters) will be favoured not because they improve survivorship or fecundity (i.e., by natural selection), but because they improve an individual's mating success. This basic idea has been broadly accepted by zoologists, but it has been contentious when applied to plants, not least because they are often hermaphrodites. In this Primer, we explain the application of sexual-selection ideas to both dioecious and hermaphroditic plants. We point out that, far from being irrelevant to their study, sexual selection to increase male mating success can be interpreted as a major selective force in the evolution of floral diversity (Figure 1).

The joint evolution of mating system and pollen performance: Predictions regarding male gametophytic evolution in selfers vs. outcrossers

Abstract Studies of sexual selection in plants historically have focused on pollinator attraction, pollen transfer, gametophytic competition, and post-fertilization discrimination by maternal plants. Pollen performance (the speeds of germination and pollen tube growth) in particular is thought to be strongly subject to intrasexual selection, but the effect of mating system on this process has not been rigorously evaluated. Here we propose four predictions derived from the logic that pollen performance should evolve with mating system as an adaptive response to: (1) the competitive environment among pollen genotypes and (2) variation among female genotypes regularly encountered by a given pollen genotype. First, as previously predicted, due to the higher potential for intense selection among diverse pollen genotypes in outcrossing relative to selfing taxa, pollen should evolve to germinate and/or to grow more rapidly in outcrossers than in selfers. Second, due to stronger selection on pollen performance in outcrossing than in selfing taxa, heritable variation in pollen tube growth rate is more likely to be purged in outcrossers. In selfers, by contrast, genetic variation in pollen tube growth rates may readily accumulate because selfing reduces the number of genetically distinct male gametophytes likely to be deposited on any given stigma, thereby relaxing selection on male gametophytic traits. A summary of published studies presented here provides preliminary support for this prediction. Third, due to the high probability that the pollen of outcrossing individuals will be exposed to multiple pistil genotypes, we predict that the pollen of habitually outcrossing taxa will evolve to perform more consistently across female genotypes than the pollen of selfing taxa. Fourth, we predict that epistatic interactions between pollen and pistil genotypes are more likely to evolve in selfers than in outcrossers. We suggest several empirical approaches that may be used to test these predictions.

Hummingbird responses to gender-biased nectar production: are nectar biases maintained by natural or sexual selection?

Pollinators mediate the evolution of secondary floral traits through both natural and sexual selection. Gender-biased nectar, for example, could be maintained by one or both, depending on the interactions between plants and pollinators. Here, I investigate pollinator responses to gender-biased nectar using the dichogamous herb Chrysothemis friedrichsthaliana (Gesneriaceae) which produces more nectar during the male floral phase. Previous research showed that the hummingbird pollinator Phaethornis striigularis visited male-phase flowers more often than female-phase flowers, and multiple visits benefited male more than female fecundity. If sexual selection maintains male-biased rewards, hummingbirds should prefer more-rewarding flowers independent of floral gender. If, however, differential rewards are partially maintained through natural selection, hummingbirds should respond to asymmetry with visits that reduce geitonogamy, i.e. selfing and pollen discounting. In plants with male biases, these visit types include single-flower visits and movements from low to high rewards. To test these predictions, I manipulated nectar asymmetry between pairs of real or artificial flowers on plants and recorded foraging behaviour. I also assessed maternal costs of selfing using hand pollinations. For plants with real flowers, hummingbirds preferred more-rewarding flowers and male-phase morphology, the latter possibly owing to previous experience. At artificial arrays, hummingbirds responded to extreme reward asymmetry with increased single-flower visits; however, they moved from high to low rewards more often than low to high. Finally, selfed flowers did not produce inferior seeds. In summary, sexual selection, more so than geitonogamy avoidance, maintains nectar biases in C. friedrichsthaliana, in one of the clearest examples of sexual selection in plants, to date.

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.

Effects of pollen load size and composition on pollen donor performance in wild radish, Raphanus sativus (Brassicaceae)

A critical concern in the debate over the importance of sexual selection in plants is whether the nonrandom mating demonstrable in greenhouse crosses can occur in the field. Field populations likely experience smaller and more variable pollen load sizes than those that have been used in many greenhouse experiments. Therefore, we performed a greenhouse experiment in which we varied both pollen load size and composition in wild radish, Raphanus sativus, and examined the paternity of seeds. We used five maternal plants and four pairs of pollen donors. We were able to produce pollen loads of 40, 118, and 258 grains per stigma. The smallest of the pollen loads was scant enough to result in a slight, but significant reduction in seed number per fruit. While variation in pollen load composition significantly affected the proportions of seeds fathered by different donors, variation in pollen load size did not. The relative performance of different donors was constant across pollen load sizes, suggesting that, for this species, differential performance of pollen donors can occur at pollen load sizes that are likely to occur in field populations.

A "Good-Sperm" Model Can Explain the Evolution of Costly Multiple Mating by Females

A "Good-Sperm" Model Can Explain the Evolution of Costly Multiple Mating by Females

DOES INTERFERENCE COMPETITION AMONG POLLEN GRAINS OCCUR IN WILD RADISH?

Interest in the possibility of sexual selection in plants has focused primarily on competition among pollen donors based on the speed of pollen-tube growth. However, when pollen arrives on stigmas, there is the opportunity for both races for access to ovules (exploitation competition) and interference with the germination and growth of pollen from other donors (interference competition). We considered whether this second form of competition might occur among pollen grains of wild radish in two experiments. In the first, interference likely occurred because the amount of pollen germination was less in mixed-donor than in single-donor pollinations. This result was duplicated in a second experiment, which also showed that interference occurred only when pollen grains from different donors were in direct contact with each other. In addition, in the second experiment, the opportunity for interference affected the frequency of seeds sired by different pollen donors. Because pollen loads are often mixed in nature, interference competition among pollen grains may be important in the ecology and evolution of plant reproduction.

Pollinator Preference for Symmetrical Flowers and Sexual Selection in Plants

Floral characters are often subject to strong directional selection from pollinators, and this may disrupt developmental homeostasis in flowers that therefore develop large degrees of fluctuating asymmetry. Fluctuating asymmetry in floral traits may lead to sexual selection in plants if pollinators assortatively visit symmetrical flowers. We studied the relationship between pollination and floral asymmetry in ten different flowering plant species in Spain, Denmark, and Sweden. Pollinators preferentially visited symmetrical flowers independently of whether the plant species produced nectar. Symmetrical flowers of some species had higher pollinator rewards in terms of nectar content than asymmetrical flowers. Handling time of flowers was unaffected by asymmetry since insect visits to symmetrical flowers lasted as long as visits to asymmetrical flowers. Insect preferences for symmetrical flowers should have resulted in sexual selection with respect to symmetry. The evolution of pollinator preferences for symmetrical flowers and the potential fitness benefits to plants with symmetrical flowers due to this preference are discussed

Sexual selection in plants: pros and cons.

Sexual selection has long been regarded as a special mode of selection in animals. Various authors have argued in a growing number of publications since 1979 that sexual selection is also operative in plants, and consequently, two divergent concepts of sexual selection are now being stated in the literature, the original Darwinian concept and the new plant-centered concept. An essential feature of the Darwinian concept is the distinction between primary and secondary sexual characters. Sexual selection is a process producing secondary sexual characters in males; such characters are well known in animals but are unknown in plants. Proponents of sexual selection in plants do not mention the subject of primary and secondary sexual characters, and they make no effort to establish the existence of secondary sexual characters in plants. The evidence they do present for sexual selection in plants consists of primary sexual characters and other reproductive traits that are products of selection modes other than sexual selection.

Sexual Selection in Plants: Perspective and Overview

Sexual selection has a long history of controversy, which shows little sign of waning. The more recent application of the concept to plants continues the historical trend. In recent years, the number of articles on sexual selection has grown; in journals that regularly accept articles on both animals and plants, the frequency of those on sexual selection in plants has grown dramatically. However, articles that examine processes and outcomes related to sexual selection in plants often do not use the term sexual selection, a tendency that indicates the aura of controversy in the field. In the decade since the last broad review of sexual selection in plants, considerable progress has been made in understanding both process and outcome of sexual selection in the botanical world. I have argued that sexual selection can occur at any phase of the reproductive process, from "courtship" to postnatal stages, in plants as well as animals. Most of this work has addressed events or traits before fertilization, but postfertilization aspects of sexual selection are receiving increased attention. As work continues, variation emerges in both pattern and process, which provides a critical investigative tool. The dynamic interplay of concept and results provides evidence of a lively, vigorous field of research.

Bateman's Principles and the Measurement of Sexual Selection in Plants and Animals

A. J. Bateman's approach to animal mating systems is generalized to provide a framework for studying sexual selection in plants and hermaphroditic animals. The key feature of this generalization is the realization that the relationship between fecundity and mating success can take a variety of forms beyond those observed in Bateman's data. Thus, under many circumstances, female animals, or the female function of a hermaphroditic plant or animal, can experience sexual selection. Path diagrams are used to show that sexual selection is a component of fecundity selection. Finally, statistical procedures are discussed for measuring sexual selection in plant and animal populations with separate or combined sexes.

Postpollination Selection and Male Fitness in Plants

Postpollination events are often described as potential mechanisms for sexual selection in plants. The broadest interpretation of what constitutes sexual selection includes selection on both pollen (analogous to sperm competition in animals) and embryos as possible manifestations of male-male competition and/or female choice. Including selective embryo abortion as a mechanism for sexual selection is controversial because interactions among young progeny and their maternal parent are distinct from interactions among parental plants or their gametes. Nonetheless, I discuss mechanisms for both pre- and postfertilization selection, in part because of the practical difficulties of discriminating between the two. I focus on whether these processes result in differential mating success among pollen donors in natural populations. Evolutionary change occurs when such differences are due to traits controlled by additive genetic variation. Little evidence suggests that postpollination mechanisms affect male reproduc...

Is there a Unifying Concept of Sexual Selection that Applies to Both Plants and Animals?

This article introduces a symposium on sexual selection in plants and animals and seeks a definition of sexual selection that applies to both kingdoms. Ten different criteria that could be used as a basis for defining sexual selection are reviewed. In particular, I argue that "mate choice" and "sexual competition" are problematic elements that should be avoided in a definition. In place of these elements, I argue for a mating success definition of sexual selection and propose that it constitutes a unifying concept that applies to both plants and animals.

Patterns of fluctuating asymmetry in flowers: Implications for sexual selection in plants

AbstractCharacters in animals used in signalling and subjected to strong directional selection often demonstrate (i) an elevated level of fluctuating asymmetry (small random deviations from bilateral symmetry) and (ii) a negative relationship between the degree of individual fluctuating asymmetry and the size of a given character. We tested these two predictions in plants since flowers are subjected to strong directional selection and are involved in signalling to pollinators, whereas leaves are supposed not to be directly involved in signalling. The overall level of fluctuating asymmetry in a number of plant species with bilaterally or radially symmetric flowers was not generally higher in floral traits than in leaves. The level of fluctuating asymmetry in plants was sometimes significantly consistent within individuals. The absolute degree of individual fluctuating asymmetry in floral traits was generally negatively related to the size of the trait, while there was a positive relationship for leaves. The degree of individual fluctuating asymmetry in floral traits was marginally negatively related to the degree of individual fluctuating asymmetry in leaf traits. These patterns of fluctuating asymmetry in plants suggest that (i) the degree of asymmetry in flowers signals different aspects of quality than does the degree of asymmetry in leaves, and that (ii) fluctuating asymmetry in flowers often reflects the phenotypic quality of individual plants.

Pollen vigour and the potential for sexual selection in plants

DISCOVERING whether paternal fecundity varies within popula-tions is crucial for evaluating whether male-male competition and/or female choice can lead to sexual selection1–3. In natural populations of plants, pollinators often deposit mixtures of 'surplus' pollen from several individuals onto receptive stigmas4–7. Therefore within-flower competition among pollen-tubes for ovules could lead to nonrandom paternal success. We found that pollen competition was common in populations of wild rose mallow (Hibiscus moscheutos). Co-occurring individuals often differed in mean pollen-tube growth rates, and this trait was correlated with the number of seeds the plants sired when pollen mixtures were applied to stigmas. Differences between pairs of individuals in pollen-tube growth rates were consistent across maternal plants, suggesting that sexual selection can occur. This unexpected varia-tion in pollen vigour could lead to nonrandom fertilization whenever pollen-tubes compete for access to ovules.

Sexual selection in plants and animals

Belated recognition of the evolutionary import of reproductive success through male function in plants has led to the application of sexual selection theory to these organisms. Recent work has shown that there are many parallels, related to sexual selection, in the reproductive processes of animals and of plants, although the proximate mechanisms and evolutionary constraints sometimes differ.