Publisher Correction: GloPL, a global data base on pollen limitation of plant reproduction.

J. H. Burns was omitted in error from the author list of the original version of this Data Descriptor. This omission has now been corrected in both the HTML and PDF versions.

GloPL, a global data base on pollen limitation of plant reproduction.

Plant reproduction relies on transfer of pollen from anthers to stigmas, and the majority of flowering plants depend on biotic or abiotic agents for this transfer. A key metric for characterizing if pollen receipt is insufficient for reproduction is pollen limitation, which is assessed by pollen supplementation experiments. In a pollen supplementation experiment, fruit or seed production by flowers exposed to natural pollination is compared to that following hand pollination either by pollen supplementation (i.e. manual outcross pollen addition without bagging) or manual outcrossing of bagged flowers, which excludes natural pollination. The GloPL database brings together data from 2969 unique pollen supplementation experiments reported in 927 publications published from 1981 to 2015, allowing assessment of the strength and variability of pollen limitation in 1265 wild plant species across all biomes and geographic regions globally. The GloPL database will be updated and curated with the aim of enabling the continued study of pollen limitation in natural ecosystems and highlighting significant gaps in our understanding of pollen limitation.

Reflections on, and visions for, the changing field of pollination ecology.

Since the launch of Ecology Letters in 1998, the field of Pollination Ecology has changed considerably in its focus. In this review, we discuss the major discoveries across the past two decades. We quantitatively synthesise the frequency by which different concepts and topics appeared in the peer-reviewed literature, as well as the connections between these topics. We then look forward to identify pressing research frontiers and opportunities for additional integration in the future. We find that there has been a shift towards viewing plant-pollinator interactions as networks and towards understanding how global drivers influence the plants, pollinators and the ecosystem service of pollination. Future frontiers include moving towards a macroecological view of plant-pollinator interactions, understanding how ecological intensification and urbanisation will influence pollination, considering other interactions, such as plant-microbe-pollinator networks, and understanding the causes and consequences of extinctions. Pollination Ecology is poised to advance our basic understanding of the ecological and evolutionary factors that shape plant-animal interactions and to create applied knowledge that informs conservation decision making.

Revisiting the dioecy-polyploidy association: alternate pathways and research opportunities.

The evolutionary transition from hermaphroditism (combined sexes) to dioecy (separate sexes) is associated with whole genome duplication (polyploidy) in several flowering plant genera. Moreover, there is evidence for transitions in the opposite direction, i.e. a loss of dioecy with an increase in ploidy. Here, we review evidence for these associations, synthesize previous ideas on the mechanism underlying the patterns and explore alternative pathways. Specifically, we examine potential ecological and genetic mechanisms, differentiated by whether ploidy or gender (functional sex expression of the plant) changes are the primary cause and whether the effect is direct or indirect. An analysis of 22 genera variable for both ploidy and gender indicates that gender monomorphism (hermaphroditism, monoecy) is more common among diploid than polyploid species, whereas gender dimorphism (dioecy, gynodioecy, subdioecy) is more frequent among polyploid species. The transition from diploid hermaphroditic to polyploid gender-dimorphic taxa may arise directly through changes in gender as a result of genome duplication through genomic rearrangements or homeologous recombination, or changes in gender may result in increased unreduced gamete production leading to polyploid formation. Alternatively, the transition may occur through the indirect effects of genome duplication on mating system and inbreeding depression, which favor selection for unisexuality, or habitat shifts associated with unisexuality may simultaneously cause increased unreduced gamete production. Novel mechanisms for transitions in the opposite direction (from dioecy to hermaphroditism with increase in ploidy) include disruption of genetic sex determination and the benefits of reproductive assurance. We highlight key questions requiring further attention and promising approaches for answering them and better clarifying the genesis of sexual system polyploidy associations. See also the sister article focusing on animals by Wertheim et al. in this themed issue.

Sex-determining chromosomes and sexual dimorphism: insights from genetic mapping of sex expression in a natural hybrid Fragaria × ananassa subsp. cuneifolia.

We studied the natural hybrid (Fragaria × ananassa subsp. cuneifolia) between two sexually dimorphic octoploid strawberry species (Fragaria virginiana and Fragaria chiloensis) to gain insight into the dynamics of sex chromosomes and the genesis of sexual dimorphism. Male sterility is dominant in both the parental species and thus will be inherited maternally, but the chromosome that houses the sex-determining region differs. Thus, we asked whether (1) the cytotypic composition of hybrid populations represents one or both maternal species, (2) the sex-determining chromosome of the hybrid reflects the location of male sterility within the maternal donor species and (3) crosses from the hybrid species show less sexual dimorphism than the parental species. We found that F. × ananassa subsp. cuneifolia populations consisted of both parental cytotypes but one predominated within each population. Genetic linkage mapping of two crosses showed dominance of male sterility similar to the parental species, however, the map location of male sterility reflected the maternal donor in one cross, but not the other. Moreover, female function mapped to a single region in the first cross, but to two regions in the second cross. Aside from components of female function (fruit set and seed set), other traits that have been found to be significantly sexually dimorphic in the pure species were either not dimorphic or were dimorphic in the opposite direction to the parental species. These results suggest that hybrids experience some disruption of dimorphism in secondary sexual traits, as well as novel location and number of quantitative trait locus (QTL) affecting sex function.

Florivory increases selfing: an experimental study in the wild strawberry, Fragaria virginiana.

Florivores are antagonists that damage flowers, and have direct negative effects on flowering and pollination of the attacked plants. While florivory has mainly been studied for its consequences on seed production or siring success, little is known about its impact on mating systems. Damage to flowers can alter pollinator attraction to the plant and may therefore modify patterns of pollen transfer. However, the consequences of damage for mating systems can take two forms: a decrease in flower number reduces opportunities for intra-inflorescence pollen deposition (geitonogamy), which, in turn, may lead to a decrease in selfing; whereas a decrease in floral display may also reduce overall visitation and thus increase the chances of self-pollination via facilitated or autonomous autogamy. We investigated the effects of damage by a bud-clipping weevil (Anthonomus signatus) in Fragaria virginiana in an experimental setting mimicking natural conditions. We found that increased damage led to an increase in selfing, a result consistent with the increased autogamy pathway. We discuss the implications of this finding and evaluate the generality of florivore-mediated mating system expression.

Genetic mapping of sex determination in a wild strawberry, Fragaria virginiana, reveals earliest form of sex chromosome.

The evolution of separate sexes (dioecy) from hermaphroditism is one of the major evolutionary transitions in plants, and this transition can be accompanied by the development of sex chromosomes. Studies in species with intermediate sexual systems are providing unprecedented insight into the initial stages of sex chromosome evolution. Here, we describe the genetic mechanism of sex determination in the octoploid, subdioecious wild strawberry, Fragaria virginiana Mill., based on a whole-genome simple sequence repeat (SSR)-based genetic map and on mapping sex determination as two qualitative traits, male and female function. The resultant total map length is 2373 cM and includes 212 markers on 42 linkage groups (mean marker spacing: 14 cM). We estimated that approximately 70 and 90% of the total F. virginiana genetic map resides within 10 and 20 cM of a marker on this map, respectively. Both sex expression traits mapped to the same linkage group, separated by approximately 6 cM, along with two SSR markers. Together, our phenotypic and genetic mapping results support a model of gender determination in subdioecious F. virginiana with at least two linked loci (or gene regions) with major effects. Reconstruction of parental genotypes at these loci reveals that both female and hermaphrodite heterogamety exist in this species. Evidence of recombination between the sex-determining loci, an important hallmark of incipient sex chromosomes, suggest that F. virginiana is an example of the youngest sex chromosome in plants and thus a novel model system for the study of sex chromosome evolution.

Genetic constraints on floral evolution: a review and evaluation of patterns.

The characteristics of flowers influence most aspects of angiosperm reproduction, including the agents of pollination and patterns of mating. Thus, a clear view of the forces that mediate floral phenotypic evolution is central to understanding angiosperm diversity. Here, we inform on the capacity for floral phenotype to respond to selection by reviewing published data on heritabilities and genetic correlations for several classes of floral traits (primary sexual, attraction, mating system) in hermaphroditic plants. We find significant heritability for all floral traits but also variation among them, as well as a tendency for heritability to vary with mating system, but not life history. We additionally test predictions stemming from life history theory (eg, negative covariation between male-female traits and flower size-flower number), and ideas concerning the extent and pattern of genetic integration between flowers and leaves, and between the sexes of dioecious and gynodioecious species. We find mixed evidence for life history tradeoffs. We find strong support for floral integration and its relation with floral morphology (actinomorphy vs zygomorphy) and for a decoupling of floral and vegetative traits, but no evidence that modular integration varies with floral morphology. Lastly, we find mixed evidence for a relationship between the level of sexual dimorphism in attraction traits and the between-sex correlation in gender dimorphic plants.

Evolutionary ecology of the prezygotic stage.

The life cycles of sexually reproducing animals and flowering plants begin with male and female gametes and their fusion to form a zygote. Selection at this earliest stage is crucial for offspring quality and raises similar evolutionary issues, yet zoology and botany use dissimilar approaches. There are striking parallels in the role of prezygotic competition for sexual selection on males, cryptic female choice, sexual conflict, and against selfish genetic elements and genetic incompatibility. In both groups, understanding the evolution of sex-specific and reproductive traits will require an appreciation of the effects of prezygotic competition on fitness.

High variability and disomic segregation of microsatellites in the octoploid Fragaria virginiana Mill. (Rosaceae).

The objectives of the present study were to develop microsatellite markers for the wild strawberry, Fragaria virginiana, to evaluate segregation patterns of microsatellite alleles in this octoploid species, and assess genetic variability at microsatellite loci in a wild population. A genomic library was screened for microsatellite repeats and several PCR primers were designed and tested. We also tested the use of heterologous primers and found that F. virginiana primers amplified products in cultivated strawberry, Fragaria x ananassa Duch. and Fragaria chiloensis. Similarly, microsatellite loci developed from cultivated strawberry also successfully amplified F. virginiana loci. We investigated four microsatellite loci in detail, three developed from F. virginiana and one from cultivated strawberry. A survey of 100 individuals from a population of F. virginiana in Pennsylvania demonstrated high heterozygosities (H(e) or gene diversity ranged from 0.80 to 0.88 per locus) and allelic diversity (12-17 alleles per locus), but individual plants had no more than two alleles per locus. Segregation patterns in parents and progeny of two controlled crosses at these four loci were consistent with disomic Mendelian inheritance. Together these findings suggest that the genome of F. virginiana is "highly diploidized" and at least a subset of microsatellite loci can be treated as codominant, diploid markers. Significant heterozygote deficiencies were found at three of the four loci for hermaphroditic individuals but for only one locus among females in this gynodioecious species.

Sex ratio represents a unique context for selection on attractive traits: consequences for the evolution of sexual dimorphism.

We explored the idea that sex ratio represents a unique context for selection on attractive traits by manipulating sex ratio and pollinator abundance in experimental populations of a gender-dimorphic wild strawberry Fragaria virginiana. We found that increasing the frequency of functional males (the pollen-bearing morph) increased the frequency of pollen-collecting syrphid flies in the pollinator assemblage, decreased pollinator visitation to less preferred morph (females), and decreased the degree of pollen limitation of females. Moreover, sex ratio influenced the strength of selection on petal size through female fitness but did not alter the strength of selection through male fitness components, suggesting that sex ratio can alter the gender bias of selection on an attractive trait. This study of context-dependent selection has important implications for the evolution of sexual dimorphism in attractive traits. First, it suggests that only certain conditions generate male-biased selection and, thus, could lead to selection-driven male-biased petal size dimorphism. Second, it suggests that flexible pollinator foraging may be an important mechanism by which sex ratio influences selection on attractive traits. Finally, it implies that variation in sex ratio could limit the evolution of sexual dimorphism and/or could maintain genetic variation in attractive traits.

Dissecting the causes of variation in intra-inflorescence allocation in a sexually polymorphic species, Fragaria virginiana (Rosaceae).

In this study we dissect the causes of variation in intra-inflorescence allocation in a sexually polymorphic species, Fragaria virginiana. We separated out the effects of resource competition during flowering from those of inflorescence architecture, as well as identified the effects of sex morph and genotype. We found position-based variation in petal length, ovule, pollen, and flower number to be influenced more by architecture than by our resource manipulations during flowering. We also found both genotype- and sex-specific intra-inflorescence patterns. Furthermore, our data indicate that the sex morph-specific intra-inflorescence patterns result from architectural modifications of the basic pattern. In fact, sex-differential intra-inflorescence patterns suggest that fitness through male and female function may be maximized by different resource distribution patterns within the inflorescence and may have been modified by past selection. Specifically, females invested heavily in ovules at positions where fruit set was most likely (primary and secondary), at the expense of flower number and allocation per flower at more distal positions. Whereas functional males invested minimally in ovules at all flower positions and produced the most abundantly flowered inflorescences, hermaphrodites, on the other hand, showed intermediate patterns, implying a compromise between sex functions. We suggest that consideration of intra-inflorescence allocation and inflorescence architecture may reveal the mechanism underlying sexual dimorphism in flower allocation and number.

Quantitative genetics of floral traits in a gynodioecious wild strawberry Fragaria virginiana: implications for the independent evolution of female and hermaphrodite floral phenotypes.

The independent evolution of floral phenotype is an important part of the process of gender specialization during the evolution of dioecy from hermaphroditism. However, we have little information on the genetic variation of floral traits in species with separate genders. Gynodioecious species (co-occurrence of females and hermaphrodites) have a breeding system intermediate between hermaphroditism and complete separation of the sexes (dioecy) and thus can provide insight into the genetic architecture underlying floral phenotype with respect to both primary (stamens and carpels) and secondary (petals) sexual traits. I used a nested breeding design to examine the potential for response to selection on floral traits and to examine whether this response would be similar in the two sex morphs of gynodioecious Fragaria virginiana. There was significant genetic variation underlying all floral traits, although narrow-sense heritabilities (ranging from -0.25 to 0.44) were, in most cases, much lower than broad-sense ones (ranging from 0.28 to 1. 53). Moreover, the sex morphs differed significantly in their heritabilities for shared traits, such as stamen length, and showed a tendency towards differing significantly in others, like carpel number and petal length. In addition, correlations between the sex morphs for these traits (ranging from 0.41 to 0.58) were significantly greater than 0, but less than 1. These results indicate that greater sexual dimorphism could evolve in this population of F. virginiana, even if selection on these traits is not divergent. However, strong developmental integration of floral traits (e.g. stamen length and petal length) and high levels of nonadditive genetic variance may represent barriers to the evolution of complete sexual dimorphism.

Indirect costs of seed production within and between seasons in a gynodioecious species.

Dimorphic species, especially those with unisexual and hermaphroditic individuals, provide an opportunity to study the dynamics of resource allocation to reproductive function. In this study, I investigated the effects of manipulating seed production on reproductive allocation within a season and between seasons in females and hermaphrodites of gynodioecious Sidalcea oregana ssp. spicata. Plants were either hand-pollinated to ensure maximum seed set (seed plants), or prohibited from pollination and seed set (no-seed plants). These treatments were effective; seed plants produced an average of 120 seeds whereas no-seed plants produced no seeds. Within a season, seed plants and no-seed plants produced similar numbers of flowers, but seed plants significantly reduced the amount of biomass allocated to each flower compared to no-seed plants. The sexual morphs differed in per-flower allocation: hermaphrodites allocated significantly more biomass to most floral structures (except to ovules) relative to females. Nonetheless, the sexual morphs exhibited similar proportional reductions in flower size in response to seed production. When allocation to floral display was characterized by petal length, the sexual morphs responded differently during the season; hermaphrodites, in both seed treatments, maintained larger petals over the season while females greatly reduced theirs. This could be interpreted as adaptive if pollen removal is positively related to petal size. In the season following the manipulations of seed production, plants which produced seeds in 1989 had reduced allocation to influorescences (and flowers) in 1990 compared to plants which did not produce seeds in 1989. A similar trend was not detected for vegetative growth between seasons. The sexual morphs did not differ significantly in their between season responses to the seed treatment.