Plant Mating Research Articles

Primary pollinator exclusion has divergent consequences for pollen dispersal and mating in different populations of a bird-pollinated tree.

Pollination by nectarivorous birds is predicted to result in different patterns of pollen dispersal and plant mating compared to pollination by insects. We tested the prediction that paternal genetic diversity, outcrossing rate and realized pollen dispersal will be reduced when the primary pollinator group is excluded from bird-pollinated plants. Pollinator exclusion experiments in conjunction with paternity analysis of progeny were applied to Eucalyptus caesia Benth. (Myrtaceae), a predominantly honeyeater-pollinated tree that is visited by native insects and the introduced Apis mellifera (Apidae). Microsatellite genotyping at 14 loci of all adult E.caesia at two populations (n=580 and 315), followed by paternity analysis of 705 progeny, revealed contrasting results between populations. Honeyeater exclusion did not significantly impact pollen dispersal or plant mating at Mount Caroline. In contrast, at the Chiddarcooping site, the exclusion of honeyeaters led to lower outcrossing rates, a threefold reduction in the average number of sires per fruit, a decrease in intermediate-distance mating and an increase in near-neighbour mating. The results from Chiddarcooping suggest that bird pollination may increase paternal genetic diversity, potentially leading to higher fitness of progeny and favouring the evolution of this strategy. However, further experimentation involving additional trees and study sites is required to test this hypothesis. Alternatively, insects may be effective pollinators in some populations of bird-adapted plants, but ineffective in others.

Self-compatibility and autonomous selfing of plants in meadow communities.

One of the most fundamental, although controversial, questions related to the evolution of plant mating systems is the distribution of outcrossing rates. Self-compatibility, and especially autonomous self-pollination, can become particularly beneficial in anthropogenically degraded habitats with impoverished pollinator assemblages and increased pollen limitation. In a hand-pollination experiment with 46 meadow plants from the Železné hory Mts., Czech Republic, we evaluated the species' ability to adopt different mating systems. For a subset of the species, we also tested seed germination for inbreeding depression. Subsequently, we analysed relationships between the species' mating systems and 12 floral and life-history traits. We found a relatively discrete distribution of the studied species into four groups. Fully and partially self-incompatible species formed the largest group, followed by self-compatible non-selfers and mixed mating species. The germination experiment showed an absence of inbreeding depression in 19 out of 22 examined species. Nectar sugar per flower, nectar sugar per shoot and dichogamy were significant associated with the mating system. Spontaneous selfing ability and self-incompatibility in species of the meadow communities had a discrete distribution, conforming to the general distribution of mating and breeding systems in angiosperms. The low frequency of spontaneous selfers and the lack of inbreeding depression at germination suggest the existence of a selection against selfing at the later ontogenetic stages. Some floral traits, such as the level of dichogamy and amount of nectar reward, may strongly impact the balance between selfing and outcrossing rates in the self-compatible species and thus shape the evolution of mating systems.

Bees may drive the reproduction of four sympatric cacti in a vanishing coastal mediterranean-type ecosystem.

BackgroundSympatric congeneric plants might share pollinators, or each species might avoid competition by evolving specialized traits that generate partitions in pollinator assemblages. In both cases, pollen limitation (a decrease in the quality and quantity of compatible reproductive pollen) can occur, driving the plant mating system to autogamy as a mechanism of reproductive assurance. We assessed the relationships between pollinator assemblages and mating systems in a group of sympatric congeneric plants. We attempted to answer the following questions: (i) How similar are pollinator assemblages among sympatric cactus species? (ii) Which mating systems do sympatric cactus species use?MethodsWe studied sympatric Eriosyce taxa that inhabit a threatened coastal strip in a mediterranean-type ecosystem in central Chile. We performed field observations on four taxa and characterized pollinators during the years 2016 and 2017. We estimated differences in the pollinator assemblages using the Bray–Curtis index. To elucidate the mating systems, we conducted hand-pollination experiments using three treatments: manual cross-pollination, automatic self-pollination, and control (unmanipulated individuals). We tested differences in seed production for statistical significance using Kruskal–Wallis analysis.ResultsEriosyce subgibbosa showed a distinctive pollinator assemblage among the sympatric species that we studied (similarity ranged from 0% to 8%); it was visited by small bees and was the only species that was visited by the giant hummingbird Patagona gigas. Pollinator assemblages were similar between E. chilensis (year 2016 = 4 species; 2017 = 8) and E. chilensis var. albidiflora (2016 = 7; 2017 = 4); however, those of E. curvispina var. mutabilis (2016 = 7; 2017 = 6) were less similar to those of the aforementioned species. E. curvispina var. mutabilis showed the highest interannual variation in its pollinator assemblage (18% similarity). Reproduction in E. subgibbosa largely depends on pollinators, although it showed some degree of autogamy. Autonomous pollination was unfeasible in E. chilensis, which depended on flower visitors for its reproductive success. Both E. chilensis var. albidiflora and E. curvispina var. mutabilis showed some degree of autogamy.DiscussionWe observed differences in pollinator assemblages between E. subgibbosa and the remaining Eriosyce taxa, which depend on hymenopterans for pollen transfer. Pollinator assemblages showed considerable interannual variation, especially those of E. subgibbosa (ornithophilous syndrome) and E. curvispina var. mutabilis (melitophilous syndrome). Autogamous reproduction in these taxa may act as a reproductive assurance mechanism when pollinator availability is unpredictable. Our study contributes to improving our understanding of the reproductive systems of ecological interactions between threatened species in a Chilean mediterranean-type ecosystem.

Geographic variation in reproductive assurance of Clarkia pulchella.

Climate can affect plant populations through direct effects on physiology and fitness, and through indirect effects on their relationships with pollinating mutualists. We therefore expect that geographic variation in climate might lead to variation in plant mating systems. Biogeographic processes, such as range expansion, can also contribute to geographic patterns in mating system traits. We manipulated pollinator access to plants in eight sites spanning the geographic range of Clarkia pulchella to investigate geographic and climatic drivers of fruit production and seed set in the absence of pollinators (reproductive assurance). We examined how reproductive assurance and fruit production varied with the position of sites within the range of the species and with temperature and precipitation. We found that reproductive assurance in C. pulchella was greatest in populations in the northern part of the species' range and was not well explained by any of the climate variables that we considered. In the absence of pollinators, some populations of C. pulchella have the capacity to increase fruit production, perhaps through resource reallocation, but this response is climate dependent. Pollinators are important for reproduction in this species, and recruitment is sensitive to seed input. The degree of autonomous self-pollination that is possible in populations of this mixed-mating species may be shaped by historic biogeographic processes or variation in plant and pollinator community composition rather than variation in climate.

Floral resource availability of Dicliptera squarrosa (Acanthaceae) and its dependence on hummingbirds for fruit formation in a forest fragment of Central Brazil

Background and aims – Hummingbirds are dependent and specialized on nectar-feeding, and many plants depend upon them for pollination. However, the degree of plant-pollinator interdependence varies greatly among species; thus, information on plant mating systems and availability of resources may help to clarify the dependence of interacting organisms. The goals of this study were to (1) quantify the floral resource available during the flowering of Dicliptera squarrosa Nees for comparison with other co-flowering ornithophilous species, and to (2) determine the importance of floral visitors for the reproductive success of this plant.Methods – Data collection was performed in a forest fragment within the urban perimeter of Catalão, Goiás, from September 2012 to August 2013. We investigated the flowering phenology, floral biology, nectar characteristics, flower visitors and mating systems of D. squarrosa. Additionally, we evaluated the amount of floral resource offered (number of flowers and energy in joules) by co-flowering ornithophilous species within an area of 6000 m2 for comparison with D. squarrosa.Key results – Dicliptera squarrosa presents flowers adapted to pollination by hummingbirds, which act as the sole pollinator group for flowers of this species. Flowering occurs from June to September and is synchronous with five other co-flowering species. During the months between July and September, D. squarrosa is the main food source for hummingbirds in the area, offering more floral resources than all of the other five ornithophilous species together. Plants of this species are self-compatible, but they depend on hummingbirds to transfer pollen; levels of autonomous autogamy were low.Conclusions – We suggest that D. squarrosa is an important species for maintaining hummingbirds in the forest fragment due to its high production of nectar resources. In addition, data on floral biology, flower visitors, and mating systems showed the importance of hummingbirds for reproduction of D. squarrosa, suggesting a mutualistic interaction between plant and hummingbirds.

Pollination insights for the conservation of a rare threatened plant species, Astragalus tragacantha (Fabaceae)

The increase in habitat fragmentation impacts plant-pollinator interactions and threatens the sustainability of plant species. Astragalus tragacantha (Fabaceae), is a rare endangered plant species along the coastal habitats where the plant populations have undergone considerable fragmentation and decline of size. Controlled pollination treatments, the observation of pollinator activity, and pollinator captures, have been conducted to study: (1) the mating system of A. tragacantha and the potential for inbreeding depression and/or outbreeding depression based on controlled pollination treatments, (2) the pollinator composition among populations using a correspondence analysis and a hierarchical clustering, and (3) the link between pollinators and the plant reproductive success using a path-analysis model. In this study, we demonstrated that this plant was not autogamous self-pollinating and depended on pollinators for its reproduction. The absence of difference between manual and open pollinations regarding the reproductive success showed an absence of pollen limitation in our populations. We showed that populations differed in the composition of their pollinator guilds. Some pollinator species were predominant in certain populations. The pollination treatments revealed the existence of a mixed mating system in A. tragacantha populations. We showed an inbreeding depression potentially linked to a predominant pollinator-facilitated selfing, and the existence of outbreeding depression between some distant populations. These differences in pollinator guild and plant mating systems among populations must be considered during the restoration of populations along the Mediterranean coastal habitats in order to enhance the reproductive success and sustainability of A. tragacantha.

Effectiveness of camera traps for quantifying daytime and nighttime visitation by vertebrate pollinators.

Identification of pollen vectors is a fundamental objective of pollination biology. The foraging and social behavior of these pollinators has profound effects on plant mating, making quantification of their behavior critical for understanding the ecological and evolutionary consequences of different pollinators for the plants they visit. However, accurate quantification of visitation may be problematic, especially for shy animals and/or when the temporal and spatial scale of observation desired is large. Sophisticated heat‐ and movement‐triggered motion‐sensor cameras (“camera trapping”) provide new, underutilized tools to address these challenges. However, to date, there has been no rigorous evaluation of the sampling considerations needed for using camera trapping in pollination research.We measured the effectiveness of camera trapping for identifying vertebrate visitors and quantifying their visitation rates and foraging behavior on Banksia menziesii (Proteaceae). Multiple still cameras (Reconyx HC 500) and a video camera (Little Acorn LTL5210A) were deployed.From 2,753 recorded visits by vertebrates, we identified five species of nectarivorous honeyeater (Meliphagidae) and the honey possum (Tarsipedidae), with significant variation in the species composition of visitors among inflorescences. Species of floral visitor showed significant variation in their time of peak activity, duration of visits, and numbers of flowers probed per visit. Where multiple cameras were deployed on individual inflorescences, effectiveness of individual still cameras varied from 15% to 86% of all recorded visits. Methodological issues and solutions, and the future uses of camera traps in pollination biology, are discussed. Conclusions and wider implications: Motion‐triggered cameras are promising tools for the quantification of vertebrate visitation and some aspects of behavior on flowers. However, researchers need to be mindful of the variation in effectiveness of individual camera traps in detecting animals. Pollinator studies using camera traps are in their infancy, and the full potential of this developing technology is yet to be realized.

Does the evolution of self-fertilization rescue populations or increase the risk of extinction?

As a major evolutionary transition in seed plants, the evolution of plant mating systems has been much debated in evolutionary ecology. Over the last 10 years, well-established patterns of evolution have emerged. On the one hand, experimental studies have shown that self-fertilization is likely to evolve in a few generations (microevolution) as a response to rapid environmental change (e.g. pollinator decline), eventually rescuing a population. On the other, phylogenetic studies have demonstrated that repeated evolution towards self-fertilization (macroevolution) leads to a higher risk of lineage extinction and is thus likely to be disadvantageous in the long term. In either case - the short-term or long-term evolution of self-fertilization (selfing) - these findings indicate that a mating system is not neutral with respect to population or lineage persistence. They also suggest that selfing can have contrasting effects depending on time scale. This raises the question of whether mating system evolution can rescue populations facing environmental change. In this review, empirical and theoretical evidence of the direct and indirect effects of mating systems on population demography and lineage persistence were analysed. A simple theoretical evolutionary rescue model was also developed to investigate the potential for evolutionary rescue through selfing. Demographic studies consistently show a short-term advantage of selfing provided by reproductive assurance, but a long-term disadvantage for selfing lineages, suggesting indirect genomic consequences of selfing (e.g. mutation load and lower adaptability). However, our theoretical evolutionary rescue model found that even in the short term, while mating system evolution can lead to evolutionary rescue, it can also lead to evolutionary suicide, due to the inherent frequency-dependent selection of mating system traits. These findings point to the importance of analysing the demographic consequences of self-fertilization in order to predict the effect of selfing on population persistence as well as take into account the indirect genomic consequences of selfing. The pace at which processes such as inbreeding depression, purging, reproductive assurance and genomic rearrangements occur after the selfing transition is the key to clarifying whether or not selfing will result in evolutionary rescue.

Floral trait variation and links to climate in the mixed-mating annual Clarkia pulchella

The benefits of self-fertilization can vary across environments, leading to selection for different reproductive strategies and influencing the evolution of floral traits. Although stressful conditions have been suggested to favour self-pollination, the role of climate as a driver of mating-system variation is generally not well understood. Here, we investigate the contributions of local climate to intraspecific differences in mating-system traits in Clarkia pulchella Pursh in a common-garden growth chamber experiment. We also tested for plastic responses to soil moisture with watering treatments. Herkogamy (anther–stigma spacing) correlated positively with dichogamy (timing of anther–stigma receptivity) and date of first flower, and northern populations had smaller petals and flowered earlier in response to experimental drought. Watering treatment alone had little effect on traits, and dichogamy unexpectedly decreased with annual precipitation. Populations also differed in phenological response to watering treatment, based on precipitation and winter temperature of their origin, indicating that populations from cool and dry sites have greater plasticity under different levels of moisture stress. While some variation in floral traits is attributable to climate, further investigation into variation in pollinator communities and the indirect effects of climate on mating system can improve our understanding of the evolution of plant mating.

Population density and size influence pollen dispersal pattern and mating system of the predominantly outcrossed Banksia nivea (Proteaceae) in a threatened ecological community

Gene flow is a critical component of plant mating systems and influences population fitness. However, pollen dispersal can be highly variable and influenced by natural and anthropogenic fragmentation. Gene flow through pollen dispersal was investigated in two populations of contrasting size and habitat context in Banksia nivea ssp. uliginosa, a rare species in the Busselton ironstone threatened ecological community of Western Australia with a naturally fragmented distribution. Paternity analysis was conducted with seven microsatellite loci to determine mating system parameters and patterns of pollen dispersal. Outcrossing was high in both populations with a similar level of selfing for both populations despite differences in population size, density and vegetation matrix. Most mating occurred within 10 m of a mother plant in the small, clumped population, while more dispersed mating, up to 50 m from a mother plant, was recorded in the large, less dense population. Our results show that population density and size are important influences on mating system parameters and level of pollen dispersal.

Demography and mating system shape the genome-wide impact of purifying selection in Arabis alpina

Plant mating systems have profound effects on levels and structuring of genetic variation and can affect the impact of natural selection. Although theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population-genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles, whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, mating system and demography shape the impact of purifying selection on genomic variation in A. alpina These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixed-mating strategies.

Sequence diversification and phylogenetic analysis of selfincompatibility specific determinant genes in Brassicaceae

It is a long history of theoretical interest in understanding the genetic causes and consequences of shifts between outcrossing and inbreeding in plant mating systems. Selfincompatibility (SI) systems genetically promote outcrossing, and its transitions to inbreeding potentially changes genetic diversity in the evolution of species. SI in the Brassicaceae family is sporophytically controlled by a single locus (S-locus), which locates the female determinant gene SRK (S-locus receptor kinase) and the male determinant gene SCR (S-locus cysteine rich). Operation of diversifying selection maintains the diversity of SRK and SCR during the evolutionary course of S haplotypes. Here we used deduced amino acid sequences of SRK and/or SCR publicly available from seven species in three genera, Brassica, Arabidopsis and Raphanus, to investigate the sequence diversification and phylogenetic distribution of S haplotypes in the Brassicaceae family. The results reveal that SCR shows higher sequence distance than SRK within or between genera, and also in the interspecific pairs of S haplotypes. Phylogenetic analysis supports the conclusion that SI has a single origin but evolves differently within the Brassicaceae. The genetic mechanisms and consequences of the loss of SI in the Brassicaceae family are discussed.

Research Article Isolation and cross-amplification of fifteen microsatellites for oil-rewarding Calceolaria species (Calceolariaceae)

Calceolaria is a diversified American genus whose species are mainly visited by oil-collecting bees, representing a highly specialized plant-pollinator system. However, although this is a unique plant system, different aspects of its ecology and evolution remain unexplored. In this study we characterized fifteen polymorphic microsatellites for four Andean Calceolaria species using next-generation sequencing. The number of alleles per locus (Na) for the study species ranged from 2 to 11, and the observed (Ho) and expected (He) heterozygosity ranged from 0 to 0.85 and 0.3 to 0.87, respectively, while FIS ranged from 0.03 to 1.0. Among the four species, C. cana showed the greatest genetic diversity, followed by C. filicaulis. C. arachnoidea and C. lanigera showed similar, lower genetic diversity. These makers are a useful tool to conduct futures studies on population structure and gene flow. Specifically, this set of markers will be helpful to estimate selfing rates as a first approximation to the understanding of the role of specialization in plant mating system evolution

Aggregate enantiostyly: Floral visitor interactions with a previously unreported form of floral display

Floral herkogamy, or the spatial separation of reproductive structures, plays an important role in the evolution of plant mating systems. One form of herkogamy is enantiostyly, or the alternate presentation of stigmas to the left and right of the floral axis. Theoretically, enantiostyly increases outcrossing rate by promoting reciprocal pollen deposition and export, but empirical evidence of this is lacking. Understanding how pollinators interact with enantiostylous flowers will illuminate the mechanisms by which enantiostyly encourages outcross pollination. We quantified style deployment within and among plants, of Allionia incarnata L. (Nyctaginaceae), a species with a new kind of enantiostyly we call “aggregate enantiostyly”. A. incarnata is the first species known to have “compound blossoms”, with different flowers each containing a left- or right-handed style. We quantify the autonomous selfing rate and describe floral visitor interactions with this unique floral structure. We found equal frequency of left- and right-handed blossoms within and among plants. Common floral visitors, Hemiargus ceraunus and Halictus sp., interacted with either anthers or stigmas, but not both, indicating effective outcrossing at the flower level. Outcrossing produced more fruits than selfing. The order in which floral visitors interacted with reproductive structures indicates that enantiostyly may increase pollen export. However, we did not find evidence that enantiostyly affected pollen deposition. Our study provides an intriguing first look at the reproductive ecology of a species with a new unique form of herkogamy, and provides evidence on the adaptive significance of enantiostyly.

Changes in floral biology and inbreeding depression in native and invaded regions of Datura stramonium.

Plant populations invading new environments might compromise their fitness contribution to the next generation, because of the lack of native specialist pollinators and/or potential mates. Thus, changes in plant mating system and traits linked to it are expected in populations colonising new environments where selection would favour selfing and floral traits that maximise reproductive output. To test this, we studied native (Mexico) and non-native (Spain) populations of the obligate sexual reproducing annual weed Datura stramonium. Flower size, herkogamy, total number of seeds per plant, number of visits by and type of pollinators, and inbreeding depression were assessed in native and non-native populations. Finally, we measured phenotypic selection on corolla size and herkogamy in each population. Flower size and herkogamy showed wide and similar variation in both ranges. However, the largest average flower size was found in one non-native population whereas the highest average positive herkogamy was detected in one native population. On average, flowers in the native range received more visits by pollinators. Hawkmoths were the main visitors in the native populations while only bees were observed visiting flowers in Spain's populations. Only in the native range was inbreeding depression detected. Selection to reduce herkogamy was found only in one native population. Absence of both inbreeding depression and selection on floral traits suggest a change in mating system of D.stramonium in a new range where generalist pollinators may be promoting high reproductive success. Selection against deleterious alleles might explain the reduction of inbreeding depression, promoting the evolution of selfing.

The Ecology of Mating and Its Evolutionary Consequences in Seed Plants

Mating in seed plants arises from interactions between plant traits and the environmental and demographic context in which individuals reside. These interactions commonly cause nonrandom mating, including selfing and promiscuous outcrossing within local neighborhoods. Shared features of seed plants, specifically immobility, hermaphroditism, and modularity, shape the essential character of mating mediated by animals, wind, and water. In addition, diverse floral strategies promote cross- and self-mating, depending on environmental circumstances. Extrinsic ecological factors influence all stages of the mating process—pollination, pollen-tube growth, ovule fertilization—as well as seed development, determining offspring quantity and quality. Traditionally, measures of plant mating systems have focused on a single axis of variation, the maternal outcrossing rate. Instead, we argue for an expanded perspective encompassing mating portfolios, which include all offspring to which individuals contribute genetically as maternal or paternal parents. This approach should expose key ecological determinants of mating-system variation and their evolutionary consequences.

NMπ-improved re-implementation of NM+, a software for estimating gene dispersal and mating patterns.

This study introduces the NMπ computer program designed for estimation of plant mating system and seed and pollen dispersal kernels. NMπ is a re-implementation of the NM+ program and provides new features such as support for multicore processors, explicit treatment of dioecy, the possibility of incorporating uniparentally cytoplasmic markers, the possibility of assessing assortative mating due to phenotypic similarity and inference about offspring genealogies. The probability model of parentage (the neighbourhood model) accounts for missing data and genotyping errors, which can be estimated along with regular parameters of the mating system. The program has virtually no restrictions with respect to a number of individuals, markers or phenotypic characters. A console version of NMπ can be run under a wide variety of operating systems, including Windows, Linux or Mac OS. For Windows users, a graphical user interface is provided to facilitate operating the software. The program, user manual and example data are available on http://www.ukw.edu.pl/pracownicy/plik/igor_chybicki/3694/.

Flower-level developmental plasticity to nutrient availability in Datura stramonium: implications for the mating system.

Studies of phenotypic plasticity in plants have mainly focused on (1) the effect of environmental variation on whole-plant traits related to the number of modules rather than on (2) the phenotypic consequences of environmental variation in traits of individual modules. Since environmental and developmental factors can produce changes in traits related to the mating system, this study used the second approach to investigate whether within-individual variation in herkogamy-related traits is affected by the environment during plant development in two populations of Datura stramonium , an annual herb with a hypothesized persistent mixed mating system, and to determine which morphological traits may promote self-fertilization. Full-sib families of two Mexican populations of D. stramonium , with contrasting ecological histories, were grown under low, mid and high nutrient availability to investigate the effects of genetic, environmental and within-plant flower position on flower size, corolla, stamen and pistil lengths, and herkogamy. Populations showed differences in familial variation, plasticity and familial differences in plasticity in most floral traits analysed. In one population (Ticumán), the effect of flower position on trait variation varied among families, whereas in the other (Pedregal) the effect of flower position interacted with the nutrient environment. Flower size varied with the position of flowers, but in the opposite direction between populations in low nutrients; a systematic within-plant trend of reduction in flower size, pistil length and herkogamy with flower position increased the probability of self-fertilization in the Pedregal population. Besides genetic variation in floral traits between and within populations, environmental variation affects phenotypic floral trait values at the whole-plant level, as well as among flower positions. The interaction between flower position and nutrient environment can affect the plant's mating system, and this differs between populations. Thus, reductions in herkogamy with flower positions may be expected in environments with either low pollinator abundance or low nutrients.

Novel Consequences of Bird Pollination for Plant Mating.

Pollinator behaviour has profound effects on plant mating. Pollinators are predicted to minimise energetic costs during foraging bouts by moving between nearby flowers. However, a review of plant mating system studies reveals a mismatch between behavioural predictions and pollen-mediated gene dispersal in bird-pollinated plants. Paternal diversity of these plants is twice that of plants pollinated solely by insects. Comparison with the behaviour of other pollinator groups suggests that birds promote pollen dispersal through a combination of high mobility, limited grooming, and intra- and interspecies aggression. Future opportunities to test these predictions include seed paternity assignment following pollinator exclusion experiments, single pollen grain genotyping, new tracking technologies for small pollinators, and motion-triggered cameras and ethological experimentation for quantifying pollinator behaviour.

Pollinator identity and spatial isolation influence multiple paternity in an annual plant

The occurrence and extent of multiple paternity is an important component of variation in plant mating dynamics. However, links between pollinator activity and multiple paternity are generally lacking, especially for plant species that attract functionally diverse floral visitors. In this study, we separated the influence of two functionally distinct floral visitors (hawkmoths and solitary bees) and characterized their impacts on multiple paternity in a self-incompatible, annual forb, Oenothera harringtonii (Onagraceae). We also situated pollinator-mediated effects in a spatial context by linking variation in multiple paternity to variation in plant spatial isolation. We documented pronounced differences in the number of paternal sires as function of pollinator identity: on average, the primary pollinator (hawkmoths) facilitated mating with nearly twice as many pollen donors relative to the secondary pollinator (solitary bees). This effect was consistent for both isolated and nonisolated individuals, but spatial isolation imposed pronounced reductions on multiple paternity regardless of pollinator identity. Considering that pollinator abundance and pollen dispersal distance did not vary significantly with pollinator identity, we attribute variation in realized mating dynamics primarily to differences in pollinator morphology and behaviour as opposed to pollinator abundance or mating incompatibility arising from underlying spatial genetic structure. Our findings demonstrate that functionally distinct pollinators can have strongly divergent effects on polyandry in plants and further suggest that both pollinator identity and spatial heterogeneity have important roles in plant mating dynamics.