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.     

Inbreeding shapes the evolution of marine invertebrates

Inbreeding is a potent evolutionary force shaping the distribution of genetic variation within and among populations of plants and animals. Yet, our understanding of the forces shaping the expression and evolution of nonrandom mating in general, and inbreeding in particular, remains remarkably incomplete. Most research on plant mating systems focuses on self-fertilization and its consequences for automatic selection, inbreeding depression, purging, and reproductive assurance, whereas studies of animal mating systems have often assumed that inbreeding is rare, and that natural selection favors traits that promote outbreeding. Given that many sessile and sedentary marine invertebrates and marine macroalgae share key life history features with seed plants (e.g., low mobility, modular construction, and the release of gametes into the environment), their mating systems may be similar. Here, we show that published estimates of inbreeding coefficients (F_IS) for sessile and sedentary marine organisms are similar and at least as high as noted in terrestrial seed plants. We also found that variation in F_IS within invertebrates is related to the potential to self-fertilize, disperse, and choose mates. The similarity of F_IS for these organismal groups suggests that inbreeding could play a larger role in the evolution of sessile and sedentary marine organisms than is currently recognized. Specifically, associations between traits of marine invertebrates and F_IS suggest that inbreeding could drive evolutionary transitions between hermaphroditism and separate sexes, direct development and multiphasic life cycles, and external and internal fertilization.     

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.     

Plant polyploidy and non-uniform effects on insect herbivores

Genomic duplication through polyploidy has played a central role in generating the biodiversity of flowering plants. Nonetheless, how polyploidy shapes species interactions or the ecological dynamics of communities remains largely unknown. Here we provide evidence from a 4 year study demonstrating that the evolution of polyploidy has reshaped the interactions between a widespread plant and three species of phytophagous moths. Our results show that polyploidy has produced non-uniform effects, with polyploids less attacked by one insect species, but significantly more attacked by two other species. These results suggest that the evolution of plant polyploidy may not generally confer uniform resistance to multiple species of insect herbivores. In the absence of such a uniform release, the extreme evolutionary success of polyploid plants is probably due to factors other than escape from herbivory. Together, these results suggest that a primary consequence of plant polyploidy may be to shape the ecological structure of plant-insect interactions, thereby providing opportunities for diversification in both plant and insect taxa.     

CSR ecological strategies and plant mating systems: outcrossing increases with competitiveness but stress‐tolerance is related to mixed mating

A number of plant traits influence the success of fertilization and reproduction in plants. Collectively these traits represent ecological syndromes that are of evolutionary significance. However, while an association between mating system and colonizing ability has been proposed, the existence of a broader relationship between mating system and a species’ position in ecological succession has not been extensively investigated. Grime's CSR theory stresses that an ecological succession can involve changes from colonizing to either competitive or stress‐tolerant strategies. How distinct dimensions of competitiveness and stress tolerance covary with mating systems has still not been considered. We designed a comparative approach to evaluate the link between mating system, life form and CSR strategies for 1996 herbaceous and woody species. We found that CSR strategies are significantly related to mating systems. Ruderal species – colonizers in early succession – were mostly selfers while more competitive species were more often outcrossers. On the other hand, greater physiological stress tolerance was associated with mixed mating systems. Outcrossing is classically expected to be advantageous for most life history strategies other than colonizers, but we suggest that reproductive assurance can counterbalance this effect in stressful environments where populations are sparse and pollinators are rare. Therefore, our results emphasize that competition and abiotic stresses are not equivalent selective pressures on the evolution of mating systems. Finally, we found plant life span to convey additional information on mating system variation, supporting its role for mating system evolution. These findings encourage further investigation of the evolutionary role of ecological strategies as syndromes of traits and suggest that the emergence of large databases of plant traits will help address the major evolutionary hypotheses on such syndromes.     

Mating system and ploidy influence levels of inbreeding depression in Clarkia (Onagraceae)

Inbreeding depression is the reduction in offspring fitness associated with inbreeding and is thought to be one of the primary forces selecting against the evolution of self-fertilization. Studies suggest that most inbreeding depression is caused by the expression of recessive deleterious alleles in homozygotes whose frequency increases as a result of self-fertilization or mating among relatives. This process leads to the selective elimination of deleterious alleles such that highly selfing species may show remarkably little inbreeding depression. Genome duplication (polyploidy) has also been hypothesized to influence levels of inbreeding depression, with polyploids expected to exhibit less inbreeding depression than diploids. We studied levels of inbreeding depression in allotetraploid and diploid species of Clarkia (Onagraceae) that vary in mating system (each cytotype was represented by an outcrossing and a selfing species). The outcrossing species exhibited more inbreeding depression than the selfing species for most fitness components and for two different measures of cumulative fitness. In contrast, though inbreeding depression was generally lower for the polyploid species than for the diploid species, the difference was statistically significant only for flower number and one of the two measures of cumulative fitness. Further, we detected no significant interaction between mating system and ploidy in determining inbreeding depression. In sum, our results suggest that a taxon's current mating system is more important than ploidy in influencing levels of inbreeding depression in natural populations of these annual plants.     

Mitosis, stature and evolution of plant mating systems: low-Phi and high-Phi plants

There is a long-recognized association in plants between small stature and selfing, and large stature and outcrossing. Inbreeding depression is central to several hypotheses for this association, but differences in the evolutionary dynamics of inbreeding depression associated with differences in stature are rarely considered. Here, we propose and test the Phi model of plant mating system evolution, which assumes that the per-generation mutation rate of a plant is a function of the number of mitoses (Phi) that occur from zygote to gamete, and predicts fundamental differences between low-Phi (small-statured) and high-Phi (large-statured) plants in the outcomes of the joint evolution of outcrossing rate and inbreeding depression. Using a large dataset of published population genetic studies of angiosperms and conifers, we compute fitted values of inbreeding depression and deleterious mutation rates for small- and large-statured plants. Consistent with our Phi model, we find that populations of small-statured plants exhibit a range of mating systems, significantly lower mutation rates, and intermediate inbreeding depression, while large-statured plants exhibit very high mutation rates and the maximum inbreeding depression of unity. These results indicate that (i) inbred progeny typically observed in large-statured plant populations are completely lost prior to maturity in nearly all populations; (ii) evolutionary shifts from outcrossing to selfing are generally not possible in large-statured species, rather, large-statured species are more likely to evolve mating systems that avoid selfing such as self-incompatibility and dioecy; (iii) destabilization of the mating system-high selfing rate with high-inbreeding depression-might be a common occurrence in large-statured species; and (iv) large-statured species in fragmented populations might be at higher risk of extinction than previously thought. Our results help to unify and simplify a large and diverse field of research, and serve to emphasize the importance that developmental and genetic constraints play in the evolution of plant mating systems.     

Purging of inbreeding depression within a population of Oxalis alpina (Oxalidaceae)

? Premise of the study: Variation among individuals in levels of inbreeding depression associated with selfing levels could influence mating system evolution by purging deleterious alleles, but empirical evidence for this association is limited. ? Methods: We investigated the association of family-level inbreeding depression and presumed inbreeding history in a tristylous population of Oxalis alpina (Oxalidaceae). ? Key results: Mid-styled individuals possessed the greatest degree of self-compatibility (SC) and produced more autogamous capsules than short- or long-styled individuals. Offspring of highly self-compatible mid-styled individuals showed reduced inbreeding depression. Mid-styled plants that produced capsules autogamously exhibited reduced stigma-anther separation compared to mid-styled plants that produced no capsules autogamously. Reduced inbreeding depression was not correlated with stigma-anther separation, suggesting that self-compatibility and autogamy evolve before morphological changes in stigma-anther separation. ? Conclusions: Purging of inbreeding depression occurred in SC mid-styled maternal families. Low inbreeding depression in SC mid-styled plants may lead to retention of the mid-styled morph in populations, despite the occurrence of higher selfing rates in mid-styled relative to short- or long-styled morphs. Variation among individuals in levels of self-fertilization within populations may lead to associations between inbreeding lineages and lower levels of inbreeding depression, influencing the evolution of mating systems.     

The demography and population genomics of evolutionary transitions to self-fertilization in plants

The evolution of self-fertilization from outcrossing has occurred on numerous occasions in flowering plants. This shift in mating system profoundly influences the morphology, ecology, genetics and evolution of selfing lineages. As a result, there has been sustained interest in understanding the mechanisms driving the evolution of selfing and its environmental context. Recently, patterns of molecular variation have been used to make inferences about the selective mechanisms associated with mating system transitions. However, these inferences can be complicated by the action of linked selection following the transition. Here, using multilocus simulations and comparative molecular data from related selfers and outcrossers, we demonstrate that there is little evidence for strong bottlenecks associated with initial transitions to selfing, and our simulation results cast doubt on whether it is possible to infer the role of bottlenecks associated with reproductive assurance in the evolution of selfing. They indicate that the effects of background selection on the loss of diversity and efficacy of selection occur rapidly following the shift to high selfing. Future comparative studies that integrate explicit ecological and genomic details are necessary for quantifying the independent and joint effects of selection and demography on transitions to selfing and the loss of genetic diversity.     

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。     

Evidence for maintenance of sex by pathogens in plants

The predominance of outcrossing despite the substantial transmission advantage of self-fertilization remains a paradox. Theory suggests that selection can favor outcrossing if it enables the production of offspring that are less susceptible to pathogen attack than offspring produced via self-fertilization. Thus, if pathogen pressure is contributing to the maintenance of outcrossing in plants, there may be a positive correlation between the number of pathogen species attacking plant species and the outcrossing rate of the plant species. We tested this hypothesis by examining the association between outcrossing rate and the number of fungal pathogen species that attack a large, taxonomically diverse set of seed plants. We show that plant species attacked by more fungal pathogen species have higher outcrossing rates than plants with fewer enemies. This relationship persists after correcting for study bias among natural and agricultural species of plants. We also accounted for the nested hierarchy of relationships among plant lineages by conducting phylogenetically independent contrasts (PICs) within genera and families that were adequately represented in our dataset. A meta-analysis of the correlation between pathogen and outcrossing PICs shows that there is a positive correlation between pathogen species number and outcrossing rates. This pattern is consistent with the hypothesis that pathogen-mediated selection may contribute to the maintenance of outcrossing in species of seed plants.     

COMPARATIVE EVIDENCE FOR THE CORRELATED EVOLUTION OF POLYPLOIDY AND SELF‐COMPATIBILITY IN SOLANACEAE

Breakdown of self‐incompatibility occurs repeatedly in flowering plants with important evolutionary consequences. In plant families in which self‐incompatibility is mediated by S‐RNases, previous evidence suggests that polyploidy may often directly cause self‐compatibility through the formation of diploid pollen grains. We use three approaches to examine relationships between self‐incompatibility and ploidy. First, we test whether evolution of self‐compatibility and polyploidy is correlated in the nightshade family (Solanaceae), and find the expected close association between polyploidy and self‐compatibility. Second, we compare the rate of breakdown of self‐incompatibility in the absence of polyploidy against the rate of breakdown that arises as a byproduct of polyploidization, and we find the former to be greater. Third, we apply a novel extension to these methods to show that the relative magnitudes of the macroevolutionary pathways leading to self‐compatible polyploids are time dependent. Over small time intervals, the direct pathway from self‐incompatible diploids is dominant, whereas the pathway through self‐compatible diploids prevails over longer time scales. This pathway analysis is broadly applicable to models of character evolution in which sequential combinations of rates are compared. Finally, given the strong evidence for both irreversibility of the loss of self‐incompatibility in the family and the significant association between self‐compatibility and polyploidy, we argue that ancient polyploidy is highly unlikely to have occurred within the Solanaceae, contrary to previous claims based on genomic analyses.     

Tempo and mode of mating system evolution between incipient Clarkia species

Mating systems are among the most labile characteristics of flowering plants, with transitions frequently occurring among populations or in association with speciation. The frequency of mating system shifts has made it difficult to reconstruct historical evolutionary dynamics unless transitions have been very recent. Here, we examine molecular and phenotypic variation to determine the polarity, timescale, and causes of a transition between outcrossing and self-fertilization in sister subspecies of Clarkia xantiana. Phylogenetic analyses and coalescent-based estimates of the time to most recent common ancestor indicated that outcrossing is ancestral to selfing and that there has been a single origin of selfing. Estimates of divergence time between outcrossing and selfing subspecies were 10,000 (95% CI [credible interval]: 3169-66,889) and 65,000 years ago (95% CI: 33,035-151,448) based on two different methods, suggesting a recent and rapid evolutionary transition. Population genetic data indicated that the transition to selfing was associated with a 80% reduction in molecular diversity, which is much greater than the 50% reduction expected under a shift from obligate outcrossing to obligate self-fertilization alone. Our data also suggest that this severe loss of diversity was caused by colonization bottlenecks. Together with previous studies, evidence for reproductive assurance in C. xantiana now connects variation in plant-pollinator interactions in the field to phenotypic and molecular evolution.     

Molecular mechanisms of self-incompatibility in flowering plants and fungi - different means to the same end

Hermaphrodite flowering plants and fungi face the same sexual dilemma - how to avoid self-fertilization. Both have evolved ingenious recognition systems that reduce or eliminate the possibility of selfing. These self-incompatibility (SI) systems offer unique opportunities to study recognition and signalling in non-animal cells and also represent model systems for studying the evolution of breeding systems at a molecular level. In this review, the authors discuss recent molecular data that predict an astonishing diversity in the cellular mechanisms of SI operating in flowering plants and fungi.     

植物交配系统的进化、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殖保障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的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。     

Pollen discounting and the evolution of selfing in Arenaria uniflora (caryophyllaceae)

Although most models of mating system evolution assign a central role to the male transmission advantage of selfing genotypes, empirical data on the male fitness consequences of increased self-pollination are still uncommon. Here, I use measures of pollen import and export by focal plants in genotyped arrays to investigate the effects of floral morphology and pollination environment on self and outcross male function. Plants from an autogamous population of Arenaria uniflora (Caryophyllaceae) exhibit complete pollen discounting relative to closely related outcrossers, as do morphologically intermediate F1 hybrids between the two populations. However, the low cumulative male fitness of hybrids probably results from reduced pollen number or competitive ability, rather than a nonlinear relationship with floral morphology. When surrounded by selfers, plants from the outcrosser population self-fertilize at nearly the same rate as selfers (>80%), but have much lower self male fitness due to reduced fruit set. Because outcross siring success is also extremely low (<8%) in this treatment, these mate-limited outcrossers are at male fitness disadvantage to both pseudocleistogamous selfers and nonlimited outcrossers. The relative male fitness of plants with different mating systems appears dependent on the ecological context, as well as on morphological trade-offs.     

An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV

Advances in recent years have revolutionized our understanding of both the context and occurrence of polyploidy in plants. Molecular phylogenetics has vastly improved our understanding of plant relationships, enabling us to better understand trait and character evolution, including chromosome number changes. This, in turn, has allowed us to appreciate better the frequent occurrence and extent of polyploidy throughout the history of angiosperms, despite the occurrence of low chromosome numbers in some groups, such as in Arabidopsis (A. thaliana was the first plant genome to be sequenced and assembled). In tandem with an enhanced appreciation of phylogenetic relationships, the accumulation of genomic data has led to the conclusion that all angiosperms are palaeopolyploids, together with better estimates of the frequency and type of polyploidy in different angiosperm lineages. The focus therefore becomes when a lineage last underwent polyploidization, rather than simply whether a plant is ‘diploid’ or ‘polyploid’. This legacy of past polyploidization in plants is masked by large‐scale genome reorganization involving repetitive DNA loss, chromosome rearrangements (including fusions and fissions) and complex patterns of gene loss, a set of processes that are collectively termed ‘diploidization’. We argue here that it is the diploidization process that is responsible for the ‘lag phase’ between polyploidization events and lineage diversification. If so, diploidization is important in determining chromosome structure and gene content, and has therefore made a significant contribution to the evolutionary success of flowering plants. © 2015 The Authors. Botanical Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of Linnean Society of London, 2016, 180 , 1–5.     

On the problems of a closed marriage: celebrating Darwin 200

Darwin devoted much of his working life to the study of plant reproductive systems. He recognized that many of the intricacies of floral morphology had been shaped by natural selection in favour of outcrossing, and he clearly established the deleterious effects of self-fertilization on progeny. Although Darwin hypothesized the adaptive significance of self-fertilization under conditions of low mate availability, he held that a strategy of pure selfing would be strongly disadvantageous in the long term. Here, I briefly review these contributions to our understanding of plant reproduction. I then suggest that investigating two very different sexual systems, one in plants and the other in animals, would throw further light on the long-term implications of a commitment to reproduction exclusively by selfing.