CONSERVATION GENETICS OF NEOTROPICAL POLLINATORS REVISITED: MICROSATELLITE ANALYSIS SUGGESTS THAT DIPLOID MALES ARE RARE IN ORCHID BEES

Allozyme analyses have suggested that Neotropical orchid bee (Euglossini) pollinators are vulnerable because of putative high frequencies of diploid males, a result of loss of sex allele diversity in small hymenopteran populations with single locus complementary sex determination. Our analysis of 1010 males from 27 species of euglossine bees sampled across the Neotropics at 2–11 polymorphic microsatellite loci revealed only five diploid males at an overall frequency of 0.005 (95% CIs 0.002–0.010); errors through genetic nondetection of diploid males were likely small. In contrast to allozyme‐based studies, we detected very weak or insignificant population genetic structure, even for a pair of populations >500 km apart, possibly accounting for low diploid male frequencies. Technical flaws in previous allozyme‐based analyses have probably led to considerable overestimation of diploid male production in orchid bees. Other factors may have a more immediate impact on population persistence than the genetic load imposed by diploid males on these important Neotropical pollinators.     

Farming practices influence wild pollinator populations on squash and pumpkin

Recent declines in managed honey bee, Apis mellifera L., colonies have increased interest in the current and potential contribution of wild bee populations to the pollination of agricultural crops. Because wild bees often live in agricultural fields, their population density and contribution to crop pollination may be influenced by farming practices, especially those used to reduce the populations of other insects. We took a census of pollinators of squash and pumpkin at 25 farms in Virginia, West Virginia, and Maryland to see whether pollinator abundance was related to farming practices. The main pollinators were Peponapis pruinosa Say; honey bees, and bumble bees (Bombus spp.). The squash bee was the most abundant pollinator on squash and pumpkin, occurring at 23 of 25 farms in population densities that were commonly several times higher than that of other pollinators. Squash bee density was related to tillage practices: no-tillage farms hosted three times as great a density of squash bees as tilled farms. Pollinator density was not related to pesticide use. Honey bee density on squash and pumpkin was not related to the presence of managed honey bee colonies on farms. Farms with colonies did not have more honey bees per flower than farms that did not keep honey bees, probably reflecting the lack of affinity of honey bees for these crops. Future research should examine the economic impacts of managing farms in ways that promote pollinators, particularly pollinators of crops that are not well served by managed honey bee colonies.     

Pollination value of male bees: the specialist bee Peponapis pruinosa (Apidae) at summer squash (Cucurbita pepo)

Male bees can be abundant at flowers, particularly floral hosts of those bee species whose females are taxonomic pollen specialists (oligolecty). Contributions of male bees to host pollination are rarely studied directly despite their prevalence in a number of pollination guilds, including those of some crop plants. In this study, males of the oligolectic bee, Peponapis pruinosa Say, were shown to be effective pollinators of summer squash, Cucurbita pepo L. Seven sequential visits from male P. pruinosa maximized squash fruit set and growth. This number of male visits accumulated during the first hour of their foraging and mate searching at flowers soon after sunrise. Pollination efficacy of male P. pruinosa and their abundances at squash flowers were sufficient to account for most summer squash production at our study sites, and by extrapolation, to two-thirds of all 87 North American farms and market gardens growing squashes that were surveyed for pollinators by collaborators in the Squash Pollinators of the Americas Survey. We posit that the substantial pollination value of male Peponapis bees is a consequence of their species' oligolecty, their mate seeking strategy, and some extreme traits of Cucurbita flowers (massive rewards, flower size, phenology).     

Biodiversity ensures plant–pollinator phenological synchrony against climate change

Climate change has the potential to alter the phenological synchrony between interacting mutualists, such as plants and their pollinators. However, high levels of biodiversity might buffer the negative effects of species‐specific phenological shifts and maintain synchrony at the community level, as predicted by the biodiversity insurance hypothesis. Here, we explore how biodiversity might enhance and stabilise phenological synchrony between a valuable crop, apple and its native pollinators. We combine 46 years of data on apple flowering phenology with historical records of bee pollinators over the same period. When the key apple pollinators are considered altogether, we found extensive synchrony between bee activity and apple peak bloom due to complementarity among bee species’ activity periods, and also a stable trend over time due to differential responses to warming climate among bee species. A simulation model confirms that high biodiversity levels can ensure plant–pollinator phenological synchrony and thus pollination function.     

Temporal analysis of the honey bee microbiome reveals four novel viruses and seasonal prevalence of known viruses, Nosema, and Crithidia

Honey bees (Apis mellifera) play a critical role in global food production as pollinators of numerous crops. Recently, honey bee populations in the United States, Canada, and Europe have suffered an unexplained increase in annual losses due to a phenomenon known as Colony Collapse Disorder (CCD). Epidemiological analysis of CCD is confounded by a relative dearth of bee pathogen field studies. To identify what constitutes an abnormal pathophysiological condition in a honey bee colony, it is critical to have characterized the spectrum of exogenous infectious agents in healthy hives over time. We conducted a prospective study of a large scale migratory bee keeping operation using high-frequency sampling paired with comprehensive molecular detection methods, including a custom microarray, qPCR, and ultra deep sequencing. We established seasonal incidence and abundance of known viruses, Nosema sp., Crithidia mellificae, and bacteria. Ultra deep sequence analysis further identified four novel RNA viruses, two of which were the most abundant observed components of the honey bee microbiome (～10(11) viruses per honey bee). Our results demonstrate episodic viral incidence and distinct pathogen patterns between summer and winter time-points. Peak infection of common honey bee viruses and Nosema occurred in the summer, whereas levels of the trypanosomatid Crithidia mellificae and Lake Sinai virus 2, a novel virus, peaked in January.     

Population structure and inbreeding in a rare and declining bumblebee, Bombus muscorum (Hymenoptera: Apidae)

Owing to habitat loss populations of many organisms have declined and become fragmented. Vertebrate conservation strategies routinely consider genetic factors, but their importance in invertebrate populations is poorly understood. Bumblebees are important pollinators, and many species have undergone dramatic declines. As monoandrous social hymenopterans they may be particularly susceptible to inbreeding due to low effective population sizes. We study fragmented populations of a bumblebee species, on a model island system, and on mainland Great Britain where it is rare and declining. We use microsatellites to study: population genetic structuring and gene flow; the relationships between genetic diversity, population size and isolation; and frequencies of (sterile) diploid males - an indicator of inbreeding. We find significant genetic structuring (theta = 0.12) and isolation by distance. Populations > 10 km apart are all significantly differentiated, both on oceanic islands and on the mainland. Genetic diversity is reduced relative to closely related common species, and isolated populations exhibit further reductions. Of 16 populations, 10 show recent bottlenecking, and 3 show diploid male production. These results suggest that surviving populations of this rare insect suffer from inbreeding as a result of geographical isolation. Implications for the conservation of social hymenopterans are discussed.     

Small wild bee abundance declines with distance into strawberry crops regardless of field margin habitat

The preservation of pollinator habitat on croplands in the form of hedgerows, wildflower strips, and natural and semi-natural areas can help maintain and enhance wild bee populations in agricultural landscapes. However, there have been few comparisons of the effectiveness of different types of field-margin pollinator habitat in maintaining bee diversity and pollination of the focal crops. We compared wild bee abundance, species richness and community composition between strawberry crops bordered by hedgerows, and those bordered by larger expanses of natural land (forests). Strawberry is an ideal crop in which to investigate pollinator export from field margins as the rows are covered with straw, which reduces habitat for ground-nesting bees within the crop; thus, most wild pollinators need to enter the crop from the margins. We sampled bees in six strawberry fields with hedgerow margins and six strawberry fields with forested margins of at least 200 m in length, using a paired design. We examined strawberry pollen deposition at regular intervals into the fields, and the magnitude of pollinator export from the field margins towards the centre of the crops. We found that bees as a group were no more species-rich or abundant in crops bordered by forests than in crops bordered by hedgerows, although large-bodied bees were more abundant in the former than the latter. Regardless of field-margin type, we found that small wild bee abundance declined significantly from the edge to the centre of the crop, but honey bee (Apis mellifera L.) and large-bodied bee abundance did not. Strawberry pollen deposition also did not decline with distance into the crop. Although previous work indicates that small wild bees are more effective (yield-increasing) pollinators of strawberry on a per-visit basis, their limited foraging ranges suggest they may only pollinate areas near the crop margins, given typical field sizes in our area.     

Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators

An adaptive role of corolla shape has been often asserted without an empirical demonstration of how natural selection acts on this trait. In generalist plants, in which flowers are visited by diverse pollinator fauna that commonly vary spatially, detecting pollinator-mediated selection on corolla shape is even more difficult. In this study, we explore the mechanisms promoting selection on corolla shape in the generalist crucifer Erysimum mediohispanicum Polatschek (Brassicaceae). We found that the main pollinators of E. mediohispanicum (large bees, small bees and bee flies) discriminate between different corolla shapes when offered artificial flowers without reward. Importantly, different pollinators prefer different shapes: bees prefer flowers with narrow petals, whereas bee flies prefer flowers with rounded overlapping petals. We also found that flowers with narrow petals (those preferred by bees) produce both more pollen and nectar than those with rounded petals. Finally, different plant populations were visited by different faunas. As a result, we found spatial variation in the selection acting on corolla shape. Selection favoured flowers with narrow petals in the populations where large or small bees are the most abundant pollinator groups. Our study suggests that pollinators, by preferring flowers with high reward, exert strong selection on the E. mediohispanicum corolla shape. The geographical variation in the pollinator-mediated selection on E. mediohispanicum corolla shape suggests that phenotypic evolution and diversification can occur in this complex floral trait even without specialization.     

Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success

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Pollination context alters female advantage in gynodioecious Silene vulgaris

Gynodioecy, the co‐occurrence of females and hermaphrodites, is arguably the most common angiosperm gender polymorphism in many florae. Females’ ability to invade and persist among hermaphrodites depends, in part, on pollinators providing adequate pollination to females. We directly measured diurnal and nocturnal pollinators’ contributions to female and hermaphrodite seed production in artificial populations of gynodioecious Silene vulgaris by experimentally restricting pollinator access. We found that female relative seed production in this system depended strongly on pollination context: females produced more than twice as many seeds as hermaphrodites in the context of abundant, nectar‐collecting moths. Conversely, females showed no seed production advantage in the context of pollen‐collecting syrphid flies and bees due to acutely hermaphrodite‐biased visitation. We infer that variation in pollinator type, behaviour and abundance may be important for achieving the female relative fitness thresholds necessary for the maintenance of gynodioecy. Generally, our study illustrates how pollinator‐mediated mechanisms may influence the evolution of breeding systems and associated suites of floral traits. Segments of a pollinator community may facilitate gynodioecy by selecting for plant characteristics that increase the attractiveness of both sexes to pollinators, such as nectar rewards. Conversely, discriminating visitors in search of pollen may restrict gynodioecy in associated plant lineages by reducing male steriles’ fitness below threshold levels.     

The population genetics of two orchid bees suggests high dispersal,low diploid male production and only an effect of island isolation in lowering genetic diversity

Orchid bees (Hymenoptera, Apidae, Euglossini) are important pollinators of many plant families in Neotropical forests, habitats that have become increasingly degraded and fragmented by agricultural practices. To understand the extent to which loss of natural habitat and isolation has affected the genetic diversity and diploid male production (DMP) of two orchid bee species, Euglossa dilemma and Euglossa viridissima, we collected and genotyped 1686 males at five microsatellite loci and tested for differences in allelic richness, heterozygosity and DMP across three different types of land use (natural, agricultural and urban) and between mainland and island populations in the Yucatan Peninsula of Mexico. We also investigated the impact of land use and geographic isolation on gene flow. Euglossa dilemma and E. viridissima seemed to be particularly resilient to loss of natural habitat; in locations with human impact, we did not find reduced genetic diversity, and populations generally showed very little population genetic structure. Only on islands did E. dilemma show significantly reduced genetic diversity. Even after accounting for putative null alleles, DMP was very low (0.2–1.3%) across all sampling sites, including on islands. We therefore suggest that DMP is an insensitive measure of inbreeding and population decline in our two study species.     

Monitoring the conservation status of bumble bee populations across an elevation gradient in the Front Range of Colorado

Bumble bees are important pollinators of native flowers and crop plants. Consequently, declines in bumble bee populations in many regions around the globe are cause for concern. We monitored abundance of 22 bumble bee species at multiple elevations over 5 years in Boulder County, Colorado. While no declines in abundance of any species were apparent over the course of the study, such a finding does not preclude prior declines in abundance. This study provides current baseline abundance data that can be used for future monitoring projects.     

The functional consequences of diversity in plant–pollinator interactions

The role of biological diversity in maintaining ecosystem functioning is a central issue in ecology. Most studies on diversity–functioning relationships have focused on ecosystem and community levels, leaving the extension of those relationships to other organization levels, such as populations, as a challenging and unsolved issue. Empirical studies have shown links between pollinator diversity and plant fecundity, suggesting that a diversity–functioning relationship at the population level may occur in pollination systems. We theoretically explored the effect of pollinator diversity on plant reproduction. We found that low pollinator diversity is beneficial when the most abundant pollinators are the most effective. In contrast, when the most effective pollinators are not the most abundant, we found an optimal value of pollinator diversity at which plant fecundity is maximized. When we parametrized our model with real data, we obtained that an increase in pollinator diversity was beneficial for the reproduction of some plants whereas it was harmful for other plants, the outcome depending exclusively on the differences in effectiveness among pollinators. Consequently, our theoretical approach suggests that in pollination systems the diversity–function relationship may be explained as the consequence of the interaction between among-pollinator differences in effectiveness and frequency of interaction, without the need to invoke additional ecological mechanisms.     

Constraints on polyploid evolution: a test of the minority cytotype exclusion principle

Polyploid evolution is often considered a mechanism of instant speciation; yet the establishment of rare tetraploids within diploid populations may be constrained by a frequency-dependent mating disadvantage (minority cytotype exclusion principle). I tested this hypothesis using experimental populations of Chamerion angustifolium (Onagraceae) that contained different proportions of tetraploids and diploids. Fitness, measured as total seed production over the entire flowering season, was calculated from a census of flower number and estimates of ovule number per flower and proportion of seed set per fruit. The fitness of tetraploids relative to diploids was frequency dependent, increasing from 0.4, when tetraploids were rare, to 0.7 when at 50% and 1.15 when they were in the majority (67%). This pattern exists because of a negative relationship between tetraploid frequency and seed set per fruit in diploids. Seed set in tetraploids was independent of cytotype frequency. The frequency-independent effect in tetraploids reflects higher assortative mating, partly because of non-random patterns of bee visitation. Bees visited a disproportionately high number of diploid inflorescences; however, the proportion of successive flights between tetraploids increased above random expectations as the frequency of tetraploids decreased. These results provide the first experimental test of frequency-dependent fitness in diploid-polyploid mixtures and suggest an important role for more gradual, population processes governing the evolution of polyploidy in natural populations.     

Eusocial bee male aggregations: spatially and temporally separated but genetically homogenous

Male insects mostly aggregate near sites where sexually reproductive virgin females are found and where mating occur. This reproductive strategy is quite common in Hymenoptera and appears to decrease the chances of inbreeding. In Hymenoptera, inbred mating frequently result in sterile diploid males. Production of diploid males may reach high proportions in small bee populations, and it usually lead to population extinction within a small number of generations. Aggregation of males during a short period of time allow the mixing of local genes. In this paper, we analyzed male aggregations of Tetragonisca angustula (Latreille) (Hymenoptera: Apidae), a eusocial stingless bee, using microsatellite molecular markers. We used population genetic statistics for haplodiploid organisms to address genetic structuring among male aggregations. Our findings indicate that, in general, male aggregations of T. angustula occurring over short time scales and in close proximity are genetically homogeneous as if a single aggregation. We conclude that T. angustula males randomly disperse within a population looking for mating chances rather than settle on a distinct male aggregation. This behavior seems to contribute to the reduction of inbreeding in this species.     

Nest Suitability,Fine-Scale Population Structure and Male-Mediated Dispersal of a Solitary Ground Nesting Bee in an Urban Landscape

Bees are the primary pollinators of flowering plants in almost all ecosystems. Worldwide declines in bee populations have raised awareness about the importance of their ecological role in maintaining ecosystem functioning. The naturally strong philopatric behavior that some bee species show can be detrimental to population viability through increased probability of inbreeding. Furthermore, bee populations found in human-altered landscapes, such as urban areas, can experience lower levels of gene flow and effective population sizes, increasing potential for inbreeding depression in wild bee populations. In this study, we investigated the fine-scale population structure of the solitary bee Colletes inaequalis in an urbanized landscape. First, we developed a predictive spatial model to detect suitable nesting habitat for this ground nesting bee and to inform our field search for nests. We genotyped 18 microsatellites in 548 female individuals collected from nest aggregations throughout the study area. Genetic relatedness estimates revealed that genetic similarity among individuals was slightly greater within nest aggregations than among randomly chosen individuals. However, genetic structure among nest aggregations was low (Nei’s G_ST = 0.011). Reconstruction of parental genotypes revealed greater genetic relatedness among females than among males within nest aggregations, suggesting male-mediated dispersal as a potentially important mechanism of population connectivity and inbreeding avoidance. Size of nesting patch was positively correlated with effective population size, but not with other estimators of genetic diversity. We detected a positive trend between geographic distance and genetic differentiation between nest aggregations. Our landscape genetic models suggest that increased urbanization is likely associated with higher levels of inbreeding. Overall, these findings emphasize the importance of density and distribution of suitable nesting patches for enhancing bee population abundance and connectivity in human dominated habitats and highlights the critical contribution of landscape genetic studies for enhanced conservation and management of native pollinators.     

Pollinator-mediated assortative mating in mixed ploidy populations of Chamerion angustifolium (Onagraceae)

Establishment of polyploid individuals within diploid populations is theoretically unlikely unless polyploids are reproductively isolated, pre-zygotically, through assortative pollination. Here, we quantify the contribution of pollinator diversity and foraging behaviour to assortative pollen deposition in three mixed-ploidy populations of Chamerion angustifolium (Onagraceae). Diploids and tetraploids were not differentiated with respect to composition of insect visitors. However, foraging patterns of the three most common insect visitors (all bees) reinforced assortative pollination. Bees visited tetraploids disproportionately often and exhibited higher constancy on tetraploids in all three populations. In total, 73% of all bee flights were between flowers of the same ploidy (2x–2x, 4x–4x); 58% of all flights to diploids and 83% to tetraploids originated from diploid and tetraploid plants, respectively. Patterns of pollen deposition on stigmas mirrored pollinator foraging behaviour; 73% of all pollen on stigmas (70 and 75% of pollen on diploid and tetraploid stigmas, respectively) came from within-ploidy pollinations. These results indicate that pollinators contribute to high rates of pre-zygotic reproductive isolation. If patterns of fertilization track pollen deposition, pollinator–plant interactions may help explain the persistence and spread of tetraploids in mixed-ploidy populations.     

Contagious parthenogenesis, automixis, and a sex determination meltdown

Because of the twofold cost of sex, genes conferring asexual reproduction are expected to spread rapidly in sexual populations. However, in reality this simple prediction is often confounded by several complications observed in natural systems. Motivated by recent findings in the Cape honey bee and in the parasitoid wasp Lysiphlebus fabarum, we explore through mathematical models the spread of a recessive, parthenogenesis inducing allele in a haplodiploid population. The focus of these models is on the intricate interactions between the mode of parthenogenesis induction through automixis and complementary sex determination (CSD) systems. These interactions may result in asexual production of diploid male offspring and the spread of the parthenogenesis-inducing allele through these males. We demonstrate that if parthenogenetic females produce a substantial proportion of male offspring, this may prevent the parthenogenesis-inducing allele from spreading. However, this effect is weakened if these diploid males are at least partially fertile. We also predict a degradation of multilocus CSD systems during the spread of parthenogenesis, following which only a single polymorphic CSD locus is maintained. Finally, based on empirical parameter estimates from L. fabarum we predict that male production in parthenogens is unlikely to prevent the eventual loss of sexual reproduction in this system.     

The endangered Iris atropurpurea (Iridaceae) in Israel: honey-bees,night-sheltering male bees and female solitary bees as pollinators

Background and Aims

The coastal plain of Israel hosts the last few remaining populations of the endemic Iris atropurpurea (Iridaceae), a Red List species of high conservation priority. The flowers offer no nectar reward. Here the role of night-sheltering male solitary bees, honey-bees and female solitary bees as pollinators of I. atropurpurea is documented.

Methods

Breeding system, floral longevity, stigma receptivity, visitation rates, pollen loads, pollen deposition and removal and fruit- and seed-set were investigated.

Key Results

The main wild pollinators of this plant are male eucerine bees, and to a lesser extent, but with the potential to transfer pollen, female solitary bees. Honey-bees were found to be frequent diurnal visitors; they removed large quantities of pollen and were as effective as male sheltering bees at pollinating this species. The low density of pollen carried by male solitary bees was attributed to grooming activities, pollen displacement when bees aggregated together in flowers and pollen depletion by honey-bees. In the population free of honey-bee hives, male bees carried significantly more pollen grains on their bodies. Results from pollen analysis and pollen deposited on stigmas suggest that inadequate pollination may be an important factor limiting fruit-set. In the presence of honey-bees, eucerine bees were low removal–low deposition pollinators, whereas honey-bees were high removal–low deposition pollinators, because they removed large amounts into corbiculae and deposited relatively little onto receptive stigmas.

Conclusions

Even though overall, both bee taxa were equally effective pollinators, we suggest that honey-bees have the potential to reduce the amount of pollen available for plant reproduction, and to reduce the amount of resources available to solitary bee communities. The results of this study have potential implications for the conservation of this highly endangered plant species if hives are permitted inside reserves, where the bulk of Oncocyclus iris species are protected.     

POLLINATOR EFFECTIVENESS AND SEED SET IN POPULATIONS OF AGALINIS STRICTIFOLIA (SCROPHULARIACEAE)

Examining variation in pollinator effectiveness and seed production resulting from single pollinator visits can provide a deeper understanding of how pollinators may influence reproduction in plant populations. When comparing populations, differences in the number of seeds produced from single pollinator visits to flowers may not always be attributable to differences in pollen deposition, but rather to differences in plant fecundity or resource availability. Pollinator effectiveness and seed production were studied for two populations over a 4-year period and were measured using single bee visit manipulations of flowers. No significant difference in pollinator effectiveness (pollen deposited on stigmas) was observed between the two populations. However, a significant difference between the two populations was observed in the number of seeds produced per flower. The Wellhouse population produced approximately three times as many seeds/flower from a single pollinator visit as did the Firefly Meadow population. Within each population, pollinators (Bombus pennsylvanicus and Apis mellifera) did not differ in the number of pollen grains deposited on stigmas or seeds produced per flower from single visit experiments. Differences in plant density, pollen viability, and ovules per flower also could not account for a significant amount of the variation. A resource augmentation experiment (water and fertilizer application) resulted in a decrease in seeds per flower per bee visit for the water treatment at the Wellhouse population only. For both populations, pollen deposition, pollen viability, and ovules per flower were unaffected by the resource augmentation. Alternative possibilities for the observed differences in seeds per flower per bee visit are discussed.