Understanding plant reproductive diversity

Flowering plants display spectacular floral diversity and a bewildering array of reproductive adaptations that promote mating, particularly outbreeding. A striking feature of this diversity is that related species often differ in pollination and mating systems, and intraspecific variation in sexual traits is not unusual, especially among herbaceous plants. This variation provides opportunities for evolutionary biologists to link micro-evolutionary processes to the macro-evolutionary patterns that are evident within lineages. Here, I provide some personal reflections on recent progress in our understanding of the ecology and evolution of plant reproductive diversity. I begin with a brief historical sketch of the major developments in this field and then focus on three of the most significant evolutionary transitions in the reproductive biology of flowering plants: the pathway from outcrossing to predominant self-fertilization, the origin of separate sexes (females and males) from hermaphroditism and the shift from animal pollination to wind pollination. For each evolutionary transition, I consider what we have discovered and some of the problems that still remain unsolved. I conclude by discussing how new approaches might influence future research in plant reproductive biology.     

The messenger matters: Pollinator functional group influences mating system dynamics

The incredible diversity of plant mating systems has fuelled research in evolutionary biology for over a century. Currently, there is broad concern about the impact of rapidly changing pollinator communities on plant populations. Very few studies, however, examine patterns and mechanisms associated with multiple paternity from cross‐pollen loads. Often, foraging pollinators collect a mixed pollen load that may result in the deposition of pollen from different sires to receptive stigmas. Coincident deposition of self‐ and cross‐pollen leads to interesting mating system dynamics and has been investigated in numerous species. But, mixed pollen loads often consist of a diversity of cross‐pollen and result in multiple sires of seeds within a fruit. In this issue of Molecular Ecology, Rhodes, Fant, and Skogen ( 2017 ) examine how pollinator identity and spatial isolation influence multiple paternity within fruits of a self‐incompatible evening primrose. The authors demonstrate that pollen pool diversity varies between two pollinator types, hawkmoths and diurnal solitary bees. Further, progeny from more isolated plants were less likely to have multiple sires regardless of the pollinator type. Moving forward, studies of mating system dynamics should consider the implications of multiple paternity and move beyond the self‐ and cross‐pollination paradigm. Rhodes et al. ( 2017 ) demonstrate the importance of understanding the roles that functionally diverse pollinators play in mating system dynamics.     

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.     

雌雄同体植物的性别干扰及其进化意义

雌雄同体植物在传粉和交配过程中两性功能存在潜在的冲突和妥协。除自交和近交衰退外,人们近年来更加强调导致配子浪费和适合度减少的繁殖代价——性别干扰。性别干扰潜在地存在于雌雄同体植物中,尤其是花粉和柱头空间位置接近而又同时成熟的两性花中。该文首先介绍了雌雄同体植物性别干扰的含义及其各种形式,进而用性别干扰理论来解释各种花部性状的适应意义,同时还回顾了植物中关于性别干扰的少数实验证据。该文强调,通常被解释为避免自交的花部机制实际上更大可能是为了避免性别干扰。从更广泛意义上,自交也可以看成是一种形式的性别干扰。     

Ecology and evolution of plant�Cpollinator interactions

Background

Some of the most exciting advances in pollination biology have resulted from interdisciplinary research combining ecological and evolutionary perspectives. For example, these two approaches have been essential for understanding the functional ecology of floral traits, the dynamics of pollen transport, competition for pollinator services, and patterns of specialization and generalization in plant–pollinator interactions. However, as research in these and other areas has progressed, many pollination biologists have become more specialized in their research interests, focusing their attention on either evolutionary or ecological questions. We believe that the continuing vigour of a synthetic and interdisciplinary field like pollination biology depends on renewed connections between ecological and evolutionary approaches.

Scope

In this Viewpoint paper we highlight the application of ecological and evolutionary approaches to two themes in pollination biology: (1) links between pollinator behaviour and plant mating systems, and (2) generalization and specialization in pollination systems. We also describe how mathematical models and synthetic analyses have broadened our understanding of pollination biology, especially in human-modified landscapes. We conclude with several suggestions that we hope will stimulate future research. This Viewpoint also serves as the introduction to this Special Issue on the Ecology and Evolution of Plant–Pollinator Interactions. These papers provide inspiring examples of the synergy between evolutionary and ecological approaches, and offer glimpses of great accomplishments yet to come.Key words: Floral traits, generalization and specialization, global change, male fitness, mating systems, multiple paternity, plant–pollinator networks, pollen and gene dispersal, pollinator behaviour, pollination syndromes, pollination webs, self-fertilization     

Consequences of clonal growth for plant mating

By affecting the number and the spatial distribution of flowering units (i.e., ramets), clonal growth can influence pollen transfer between plants and thus affect mating opportunities. In this paper I review some recent work that attests the importance of clonal growth for pollination patterns. A major aspect concerns the increase in floral display through the multiplication of flowering ramets. Although large floral displays can enhance pollinator attraction and may thus promote outcrossing, they can also increase rates of geitonogamy (i.e., pollination between flowers in the same plant). However, the latter aspect will depend on clonal architecture, a feature that greatly varies among clonal plant species. Future experimental studies and comparative analyses of rates of geitonogamy in species with clumped and intermingled distribution may allow for the evaluation of evolutionary interaction between clonal growth and floral traits that regulate mating patterns.     

Plant population dynamics, pollinator foraging, and the selection of self-fertilization

Many flowering plants rely on pollinators, self-fertilization, or both for reproduction. We model the consequences of these features for plant population dynamics and mating system evolution. Our mating systems-based population dynamics model includes an Allee effect. This often leads to an extinction threshold, defined as a density below which population densities decrease. Reliance on generalist pollinators who primarily visit higher density plant species increases the extinction threshold, whereas autonomous modes of selfing decrease and can eliminate the threshold. Generalist pollinators visiting higher density plant species coupled with autonomous selfing may introduce an effect where populations decreasing in density below the extinction threshold may nonetheless persist through selfing. The extinction threshold and selfing at low density result in populations where individuals adopting a single reproductive strategy exhibit mating systems that depend on population density. The ecological and evolutionary analyses provide a mechanism where prior selfing evolves even though inbreeding depression is greater than one-half. Simultaneous consideration of ecological and evolutionary dynamics confirms unusual features (e.g., evolution into extinction or abrupt increases in population density) implicit in our separate consideration of ecological and evolutionary scenarios. Our analysis has consequences for understanding pollen limitation, reproductive assurance, and the evolution of mating systems.     

Reciprocal style polymorphisms are not easily categorised: the case of heterostyly in Lithodora and Glandora (Boraginaceae)

Interest in reciprocal floral polymorphisms, such as heterostyly, has increased in recent decades because they can be used as suitable model systems to study mechanisms of outbreeding and disassortative mating in plants. Heterostylous plants are characterised by the presence of discrete morphs that differ in sex organ position and in some other ancillary traits. As regards sex organ deployment, different types of polymorphisms have been described, depending on number and type of discrete classes present in populations and degree of reciprocity between them. However, a clear-cut characterisation of stylar polymorphisms does not appear to be the best approach when there is great variability among populations because of continuous variation of some of traits examined. A recent study in Lithodora sensu lato (recently split into two separate genera, Lithodora and Glandora) showed a wide variation in sex organ position across species in the genus, which warrants precise population analysis of stylar polymorphism and its reciprocity. We provide a detailed morphometric analysis of flower sexual traits and include those considered to be ancillary characters. We report a wide variation in these traits in populations of Lithodora s.l. and highlight the subjectivity of the former characterisation of style polymorphism based on visual inspection. Ancillary traits appear repeatedly in Lithodora and Glandora, particularly in the latter. The appearance of these traits seems to be related to greater reciprocity between sexual whorls in Glandora, with the exception of G.?prostrata. These results agree with evolutionary steps proposed in the build-up of heterostyly according to some evolutionary models. We also examined variation in polymorphisms in light of current models for evolution of heterostyly, and, more specifically, we sought to verify the prediction that flower traits as a whole (i.e., flower integration) respond to selective pressure to assure the exact location of pollen on the pollinator body. Most reciprocal populations and species, where between-morph pollen transfer is expected to be higher, would show greater integration. Our results confirm this hypothesis.     

The evolution of self-fertility in apomictic plants

Self-fertilization and apomixis have often been seen as alternative evolutionary strategies of flowering plants that are advantageous for colonization scenarios and in bottleneck situations. Both traits have multiple origins, but different genetic control mechanisms; possible connections between the two phenomena have long been overlooked. Most apomictic plants, however, need a fertilization of polar nuclei for normal seed development (pseudogamy). If self-pollen is used for this purpose, self-compatibility is a requirement for successful pollen tube growth. Apomictic lineages usually evolve from sexual self-incompatible outcrossing plants, but pseudogamous apomicts frequently show a breakdown of self-incompatibility. Two possible pathways may explain the evolution of SC: (1) Polyploidy not only may trigger gametophytic apomixis, but also may result in a partial breakdown of SI systems. (2) Alternatively, frequent pseudo self-compatibility (PSC) via aborted pollen may induce selfing of pseudogamous apomicts (mentor effects). Self-fertile pseudogamous genotypes will be selected for within mixed sexual–apomictic populations because of avoidance of interploidal crosses; in founder situations, SC provides reproductive assurance independent from pollinators and mating partners. SI pseudogamous genotypes will be selected against in mixed populations because of minority cytotype problems and high pollen discounting; in founder populations, SI reactions among clone mates will reduce seed set. Selection for SC genotypes will eliminate SI unless the apomict maintains a high genotypic diversity and thus a diversity of S-alleles within a population, or shifts to pollen-independent autonomous apomixis. The implications of a breakdown of SI in apomictic plants for evolutionary questions and for agricultural sciences are being discussed.     

How pollinator-mediated mating varies with population size in plants

In most higher plants sexual interactions are mediated by animal pollinators that affect the number and differential reproductive success of mates. The number and sex of breeding individuals in populations are central factors in evolutionary theory, but the quantitative effect of plant population size on pollinator-mediated mating is understudied. We investigated variation in pollen removal (male function) and fruit set (female function) among flowering populations of different size of two bumblebee-and one butterfly-pollinated, rewardless, pollen-limited, hermaphroditic orchid species in Sweden. As the amount of pollen removed from plants by insects (either absolute or proportional) increased, so did the number of pollinations, whereas the proportions of plants with different pollinator-designated functional sex (male, female, hermaphrodite) depended primarily on the ratio between the amount of fruit set and pollen removed within populations. A larger population size was found to have several effects: (1) the total numbers of pollinia removed and fruits set increased; (2) the proportion of pollen removed from plants decreased; (3) the proportion of flowers pollinated decreased in the butterfly-but was not affected in the bumblebee-pollinated species; (4) the ratio between fruits set and pollinia removed increased linearly in the bumblebee-pollinated species but reached a maximum at c. 80 individuals in the butterfly-pollinated species; (5) the numbers of pollinator-designated pure male and hermaphrodite individuals increased; and (6) the variance in pollinium removal, but not fruit set, increased among individuals. These findings empirically verify the basic importance of population size for the mating structure of outcrossing plants, and indicate that selection for female sexual traits is reinforced when population size is smaller while selection for male sexual traits is reinforced when population size is larger.     

Real-time patterns of pollen flow in the wild-service tree, Sorbus torminalis (Rosaceae). III. Mating patterns and the ecological maternal neighborhood

Understanding the role of mother plants as pollen recipients in shaping mating patterns is essential for understanding the evolution of populations and in particular to predict the consequence of habitat fragmentation. Here, we investigated variation in mating patterns due to maternal phenotypic traits, phenological variance, and landscape features in Sorbus torminalis, a hermaphroditic, insect-pollinated and low-density, European temperate forest tree. The diversity and composition of pollen clouds received by maternal trees in S. torminalis were mainly determined by their conspecific neighborhood: isolated individuals sample more diversity through more even paternal contributions, low relatedness among paternal genes, and high rates of long-distance pollen dispersal within their progenies. Maternal phenotypic traits related to pollinator attractiveness also had an effect, but only when competition was strong: in this case, larger mother trees with more flowers sampled more diversity. The floral architecture of S. torminalis, with multiple-seeded fruit, strongly shaped mating patterns, with higher levels of correlated paternity among seeds belonging to the same fruit (30% full sibs) than among seeds belonging to different fruits (14% full sibs). Finally, flowering phenology affected the distribution of diversity among maternal pollen clouds, but the earliest and latest mother trees did not receive less diversity of pollen than the others.     

植物交酸系统的进化、资源分配对策与遗传多样性

影响植物自交率进化的选择力量主要体现在两个方面：当外来花粉量不足时,自交可以提高植物的结实率,即雌性适合度（繁殖保障）;而如果进行自交的花粉比异交花粉更易获得使胚珠受精的机会,那么自交也可以提高植物的雄性适合度（自动选择优势）。但是,鉴别什么时候是繁殖保障、什么时候是自动选择优势导致了自交的进化却是极其困难的。花粉贴现降低了自交植物通过异交花粉途径获得的适合度,即减弱了自动选择优势,而近交衰退既减少了自动选择优势也减少了繁残给自交者带来的利益。具有不同交配系统的植物种群将具有不同的资源分配对策。理论研究已经说明,自交率增加将减少植物对雄性功能的资源分配比例,但将使繁殖分配加大,而且在一定条件下交配系统在改变甚至可以导致植物生活史发生剧烈变化,即从多年生变为一年生。文献中支持自交减少植物雄性投入的证据有很多,但是对繁殖分配与自交率的关系目前还没有系统的研究,资源分配理论可以解释植物繁育系统的多样性,尤其是能够3说明为什么大多数植物都是雌雄同体的,自交对植物种群遗传结构的影响是减少种群内的遗传变异,增加种群间的遗传分化,长期以来人们一直猜测,自交者可能会丢掉一些长期进化的潜能,目前这个假说得到了一些支持。     

被子植物性系统及其可塑性

繁殖是生物适合度的最终表现,有性繁殖相关性状的多态性极大地促进了物种分化和生物多样性的维持,并影响着植物对环境变化的响应。在种群水平上,被子植物的花有雌花、雄花和两性花三种性表型,三种性表型在种群中的分布和频率即定义了种群的性系统。被子植物的性系统包含植物影响性分配和交配的相关特性,决定着雌配子、雄配子在种群中的频率、交配机会及交配方式,是有性繁殖的关键性状,在被子植物中表现出丰富的多态性,在种群水平上分为性单态和性多态两大类。性单态为被子植物的古老性状,而性多态在100多个被子植物科中独立进化产生。被子植物性系统多态性及其变化机理一直是进化生物学与生态学的热点问题之一。该文以种群水平的性多态为对象,总结了被子植物性系统的类型、表达的遗传基础、分布频率,以及遗传因子、非生物环境和交配环境对性系统表达和性分配的影响。     

花柱卷曲性异交机制及其进化生态学意义

 有花植物具有纷繁复杂的繁育系统,以避免或促进自交或异交。花柱卷曲性异交机制(Flexistyly)是最近在热带山姜属(Alpinia)植物中发现的一种促进异交的行为机制。具有这一机制的种类其自然种群中的个体根据开花行为的不同分为两种表型：一种上午散发花粉而其柱头向上反卷,远离昆虫拜访的通道;另一种其柱头上午垂向唇瓣,能够接受拜访昆虫的传粉,但自身的花药却不打开。到中午时分,两种表型花通过互为相反的柱头卷曲运动转换性别——前者柱头向下卷曲,后者柱头向上卷曲且花药打开。每朵花的花期为12 h,两种表型在自然种     

Disassortative mating and the maintenance of sexual polymorphism in painted maple

Since Darwin's pioneering research on plant reproductive biology (e.g. Darwin 1877), understanding the mechanisms maintaining the diverse sexual strategies of plants has remained an important challenge for evolutionary biologists. In some species, populations are sexually polymorphic and contain two or more mating morphs (sex phenotypes). Differences in morphology or phenology among the morphs influence patterns of non-random mating. In these populations, negative frequency-dependent selection arising from disassortative (intermorph) mating is usually required for the evolutionary maintenance of sexual polymorphism, but few studies have demonstrated the required patterns of non-random mating. In the current issue of Molecular Ecology, Shang et al. (2012) make an important contribution to our understanding of how disassortative mating influences sex phenotype ratios in Acer pictum subsp. mono (painted maple), a heterodichogamous, deciduous tree of eastern China. They monitored sex expression in 97 adults and used paternity analysis of open-pollinated seed to examine disassortative mating among three sex phenotypes. Using a deterministic 'pollen transfer' model, Shang et al. present convincing evidence that differences in the degree of disassortative mating in progeny arrays of the sex phenotypes can explain their uneven frequencies in the adult population. This study provides a useful example of how the deployment of genetic markers, demographic monitoring and modelling can be integrated to investigate the maintenance of sexual diversity in plants.     

Pollen limitation,species’ floral traits and pollinator visitation: different relationships in contrasting communities

Failures in the process of pollen transfer among conspecific plants can severely impact female reproductive success. Thus, pollen limitation can cause selection on plant mating systems and floral traits. The relationships between pollen limitation and floral traits might be partly mediated by the quantity and identity of pollinator visits. However, very little is known about the relationship between pollinator visits and pollen limitation. We examined the relationships between pollen limitation and floral traits at the community level to connect them to community ecology processes. We used 48 plant species from two contrasting communities: one species‐rich lowland community and one species‐poor alpine community. In addition, we calculated visitation rates and ecological pollination generalization for 38 of the species to examine the relationship between pollinator visitation and pollen limitation at the community level. We found low overall levels of pollen limitation that did not differ significantly between the alpine and the lowland community. In both communities, species with evolutionary specialized flowers were more pollen limited than species with unspecialized flowers. Species’ visitation rates and selfing capability were negatively related to pollen limitation in the alpine community, where pollinators are scarcer. However, flower size/number, ecological generalization of plants and flowering onset had greater effects on pollen limitation levels at the lowland community, indicating that the identity of the visitors and plant‐plant competitive interactions are more decisive for plant reproduction in this species‐rich community. There, pollen limitation increased with flower size and flowering onset, and decreased with ecological generalization, but only in species with evolutionary specialized flowers. Our study suggests that selection on plant mating system and floral traits may be idiosyncratic to each particular community and highlights the benefits of conducting community‐level studies for a better understanding of the processes underlying evolutionary responses to pollen limitation.     

High outcrossing rates in fields with mixed sorghum landraces: how are landraces maintained?

The effect of mating system on genetic diversity is a major theme in plant evolutionary genetics, because gene flow plays a large role in structuring the genetic variability within and among populations. Understanding crop mating systems and their consequences for gene flow can aid in managing agricultural systems and conserving genetic resources. We evaluated the extent of pollen flow, its links with farming practices and its impact on the dynamics of diversity of sorghum in fields of Duupa farmers in Cameroon. Duupa farmers grow numerous landraces mixed in a field, a practice that favours extensive pollen flow. We estimated parameters of the mating system of five landraces representative of the genetic diversity cultivated in the study site, using a direct method based on progeny array. The multilocus outcrossing rate calculated from all progenies was 18% and ranged from 0 to 73% among progenies. Outcrossing rates varied greatly among landraces, from 5 to 40%. Our results also showed that individual maternal plants were usually pollinated by more than eight pollen donors, except for one landrace (three pollen donors). Although the biological traits of sorghum (inflorescence morphology, floral traits, phenology) and the spatial planting practices of Duupa farmers led to extensive pollen flow among landraces, selection exerted by farmers appears to be a key parameter affecting the fate of new genetic combinations from outcrossing events. Because both natural and human-mediated factors shape evolution in crop populations, understanding evolutionary processes and designing in situ conservation measures requires that biologists and anthropologists work together.     

Heterostyly accelerates diversification via reduced extinction in primroses

The exceptional species diversity of flowering plants, exceeding that of their sister group more than 250-fold, is especially evident in floral innovations, interactions with pollinators and sexual systems. Multiple theories, emphasizing flower–pollinator interactions, genetic effects of mating systems or high evolvability, predict that floral evolution profoundly affects angiosperm diversification. However, consequences for speciation and extinction dynamics remain poorly understood. Here, we investigate trajectories of species diversification focusing on heterostyly, a remarkable floral syndrome where outcrossing is enforced via cross-compatible floral morphs differing in placement of their respective sexual organs. Heterostyly evolved at least 20 times independently in angiosperms. Using Darwin''s model for heterostyly, the primrose family, we show that heterostyly accelerates species diversification via decreasing extinction rates rather than increasing speciation rates, probably owing to avoidance of the negative genetic effects of selfing. However, impact of heterostyly appears to differ over short and long evolutionary time-scales: the accelerating effect of heterostyly on lineage diversification is manifest only over long evolutionary time-scales, whereas recent losses of heterostyly may prompt ephemeral bursts of speciation. Our results suggest that temporal or clade-specific conditions may ultimately determine the net effects of specific traits on patterns of species diversification.     

The total opportunity for sexual selection and the integration of pre‐ and post‐mating episodes of sexual selection in a complex world

It is well known that sexual selection can target reproductive traits during successive pre‐ and post‐mating episodes of selection. A key focus of recent studies has been to understand and quantify how these episodes of sexual selection interact to determine overall variance in reproductive success. In this article, we review empirical developments in this field but also highlight the considerable variability in patterns of pre‐ and post‐mating sexual selection, attributable to variation in patterns of resource acquisition and allocation, ecological and social factors, genotype‐by‐environment interaction and possible methodological factors that might obscure such patterns. Our aim is to highlight how (co)variances in pre‐ and post‐mating sexually selected traits can be sensitive to changes in a range of ecological and environmental variables. We argue that failure to capture this variation when quantifying the opportunity for sexual selection may lead to erroneous conclusions about the strength, direction or form of sexual selection operating on pre‐ and post‐mating traits. Overall, we advocate for approaches that combine measures of pre‐ and post‐mating selection across contrasting environmental or ecological gradients to better understand the dynamics of sexual selection in polyandrous species. We also discuss some directions for future research in this area.