Chromosome-Level Assembly and Annotation of the Genome of the Endangered Giant Patagonian Bumble Bee Bombus dahlbomii.

This article describes a genome assembly and annotation for Bombus dahlbomii, the giant Patagonian bumble bee. DNA from a single, haploid male collected in Argentina was used for PacBio (HiFi) sequencing, and Hi-C technology was then used to map chromatin contacts. Using Juicer and manual curation, the genome was scaffolded into 18 main pseudomolecules, representing a high-quality, near chromosome-level assembly. The sequenced genome size is estimated at 265 Mb. The genome was annotated based on RNA sequencing data of another male from Argentina, and BRAKER3 produced 15,767 annotated genes. The genome and annotation show high completeness, with >95% BUSCO scores for both the genome and annotated genes (based on conserved genes from Hymenoptera). This genome provides a valuable resource for studying the biology of this iconic and endangered species, as well as for understanding the impacts of its decline and designing strategies for its preservation.

Darwin's inflorescence syndrome is indeed associated with bee pollination.

KEY MESSAGE: A relationship between vertical acropetal inflorescences with protandrous flowers and bee pollination was hypothesized by Darwin back in 1877. Here we provide empirical evidence supporting this association across the angiosperms. Plant reproduction is not only determined by flower traits but also by the arrangement of flowers within inflorescences. Based on his observations of the orchid Spiranthes autumnalis, Darwin proposed in 1877 that bee-pollinated plants presenting protandrous flowers on vertical acropetal inflorescences, where proximal flowers open first, can exploit the stereotypical foraging behavior of their pollinators (i.e., upward movement through the inflorescence) to promote pollen exportation and reduce self-pollination. In these inflorescences, male-phase flowers lie spatially above female-phase flowers. To examine this untested hypothesis, we compiled literature information from 718 angiosperms species and evaluated the association between vertical acropetal inflorescences with protandrous flowers and bee pollination within a phylogenetic comparative framework. Results reveal that this type of inflorescence is indeed more common in species pollinated by bees. Moreover, this association does not seem to be weakened by the presence of alternative self-pollination avoidance mechanisms, like self-incompatibility, suggesting that this inflorescence type benefits mainly male rather than female fitness. Other inflorescence types placing male-phase flowers above female-phase flowers, e.g., vertical basipetal inflorescences with protogynous flowers, do not provide strong evidence of a differential association with pollination by bees. Female-biased nectar production in vertical acropetal inflorescences with protandrous flowers may reinforce the behavior of bees to fly upwards, rendering Darwin's configuration more adaptive than other inflorescence configurations.

Clinal versus disruptive latitudinal variation in fruit traits of a South American mistletoe.

Fruit traits have historically been interpreted as plant adaptations to their seed dispersers. On the other hand, different environmental factors, which vary spatially and temporally, can shape fruit-trait variation. The mistletoe Tristerix corymbosus has a latitudinal distribution along the South American Pacific rim that encompasses two different biomes, the matorral of central Chile and the temperate forest that extends south of the matorral. This mistletoe shows contrasting fruiting phenology (spring vs summer), fruit color (yellow vs green), and seed dispersers (birds vs marsupial) in these two biomes. We characterized geographic variation of morphological and nutritional fruit traits of T. corymbosus to evaluate which macroecological factor, biome or latitude, better explains spatial variation in these variables. For each of 22 populations, we obtained environmental data (temperature, precipitation, and canopy cover), measured fruit and seed morphology traits (size, shape, and weight), and pulp moisture and nutritional content (fiber, protein, fat, carbohydrates, ash, and caloric content). Patterns of variation for each variable were described by fitting and comparing five different simple models varying in slope, intercept or both. Fruit morphology showed a clear biome-related disruptive pattern, seed morphological traits were unrelated to either biome or latitude, whereas nutritional variables showed diverse patterns. Different environmental factors seem to affect fruit development and phenology, determining the observed fruit characteristics, with seed dispersers playing a minor role in shaping these patterns. More generally, the contrasting plant-seed disperser associations we addressed can be interpreted as the outcome of an ecological-fitting rather than of a coevolutionary process.

Managed honeybees decrease pollination limitation in self-compatible but not in self-incompatible crops.

Modern agriculture is becoming increasingly pollinator-dependent. However, the global stock of domesticated honeybees is growing at a slower rate than its demand, while wild bees are declining worldwide. This uneven scenario of high pollinator demand and low pollinator availability can translate into increasing pollination limitation, reducing the yield of pollinator-dependent crops. However, overall assessments of crop pollination limitation and the factors determining its magnitude are missing. Based on 52 published studies including 30 crops, we conducted a meta-analysis comparing crop yield in pollen-supplemented versus open-pollinated flowers. We assessed the overall magnitude of pollination limitation and whether this magnitude was influenced by (i) the presence/absence of managed honeybees, (ii) crop compatibility system (i.e. self-compatible/self-incompatible) and (iii) the interaction between these two factors. Overall, pollen supplementation increased yield by approximately 34%, indicating sizable pollination limitation. Deployment of managed honeybees and self-compatibility were associated with lower pollination limitation. Particularly, active honeybee management decreased pollination limitation among self-compatible but apparently not among self-incompatible crops. These findings indicate that current pollination regimes are, in general, inadequate to maximize crop yield, even when including managed honeybees, and stress the need of transforming the pollination management paradigm of agricultural landscapes.

Behavioural responses by a bumble bee to competition with a niche-constructing congener.

While feeding, foragers can alter their environment. Such alteration constitutes ecological niche construction (ENC) if it enables future benefits for the constructor and conspecific individuals. The environmental modification may also affect non-constructing, bystander species, especially if they share resources with constructor species. If so, ENC could confer the constructor species a competitive advantage by both enhancing its foraging returns and reducing those of bystander species. Expectations - (E1) ENC frequency should vary positively with the recent and current density of the constructor species, and (E2) constructors should use modifications disproportionately. In contrast, bystanders should (E3) experience intensified competition for the affected resource, and (E4) exhibit diverse, possibly mitigating, responses to ENC, depending on opportunity and relative benefits. We investigated these expectations in Argentina for competition for Fuchsia magellanica nectar between an invasive bumble bee Bombus terrestris (terr: putative constructor), which often bites holes at the bases of floral tubes to rob nectar, and native B. dahlbomii (dahl: bystander), which normally accesses Fuchsia nectar through the flower mouth (front visits). Robbing holes constitute ENC, as they persist until the 7-day flowers wilt. The dynamics of the incidence of robbed flowers, abundance of both bees and the number and types of their flower visits (front or robbing) were characterised by alternate-day surveys of plants during 2.5 months. After initially accessing Fuchsia nectar via front visits, terr switched to robbing and its abundance on Fuchsia increased 20-fold within 10 days (E2). Correspondingly, the incidence of robbed flowers varied positively with recent and past terr abundance (E1). In contrast, dahl abundance remained low and varied negatively with the incidence of robbed flowers (E3). When terr ceased visiting Fuchsia, dahl abundance increased sixfold within 10 days (E3), possibly because many dahl previously had avoided competition with terr by feeding on other plant species (E4). While terr was present, dahl on Fuchsia used front visits (tolerance) or used existing robbing holes (adoption: E4). The diverse dahl responses suggest partial compensation for competition with terr. ENC alters competitive asymmetry, favouring constructor species. However, bystander responses can partially offset this advantage, perhaps facilitating coexistence.

Los animales pueden alterar su ambiente como consecuencia del forrajeo. Esta alteración constituye una forma de construcción de nicho ecológico (CNE) cuando la misma promueve beneficios para el constructor y otros individuos de la misma especie. Esta modificación ambiental puede también afectar otras especies no involucradas directamente en la CNE, especialmente cuando comparten recursos con la especie constructora. En este caso, la CNE puede conferir una ventaja competitiva a la especie constructora, incrementado sus beneficios alimenticios en detrimento de los de las especies no constructoras. Expectativas - (E1) La frecuencia de eventos de CNE debería variar positivamente con la densidad presente y pasada de la especie constructora, y (E2) los individuos de la especie constructora deberían usar las modificaciones asociadas a la CNE en forma diferencial. Por el contrario, los individuos de las otras especies que usen el mismo recurso deberían (E3) experimentar una intensificación de la competencia, y (E4) exhibir una diversidad de respuestas, algunas que atenúen las consecuencias negativas de la CNE, lo que va a depender de la oportunidad y de los beneficios relativos. En Argentina, investigamos el cumplimiento de estas expectativas en la competencia por el néctar de Fuchsia magellanica entre el abejorro invasor, Bombus terrestris (terr: la especie constructora), quien frecuentemente agujerea la base de tubos florales para robar néctar, y el abejorro nativo B. dahlbomii (dahl: la especie afectada), quien normalmente accede al néctar de Fuchsia en forma legítima a través de la apertura de la flor (visitas frontales). Los agujeros realizados por terr constituyen un caso de CNE, ya que persisten a lo largo de la vida de la vida de la flor (aprox. 7-day). En este trabajo relevamos la incidencia de flores robadas, la abundancia de las dos especies de abejas, y el número y tipo de sus visitas florales (frontales o de robo) día por medio durante 2.5 meses. Inicialmente terr accedió las flores de Fuchsia frontalmente, pero más tarde cambió su comportamiento convirtiéndose en un robador casi exclusivo a lo largo de un período de 10 días en que su abundancia se incrementó 20 veces (E2). En consecuencia, la incidencia de flores robadas varió positivamente con la abundancia de terr presente y pasada (E1). Por el contrario, la abundancia de dahl fue baja y varió negativamente con la incidencia de flores robadas (E3). En particular, la abundancia de dahl se incrementó seis veces en un período de 10 días una vez que terr cesó de visitar las flores de Fuchsia (E3), posiblemente porque dahl evitó la competencia con terr forrajeando en otras especies de plantas (E4). Cuando terr estuvo presente, dahl visitó las flores de Fuchsia frontalmente (tolerancia) o usó los agujeros existentes (adopción de comportamiento robador: E4). Estas respuestas diversas de dahl sugieren una compensación parcial de los efectos negativos de la competencia con terr. La CNE incrementa la asimetría de la competencia, favoreciendo la especie constructora. Sin embargo, las diferentes respuestas de las especies afectadas pueden compensar parcialmente esta desventaja competitiva, tal vez facilitando la coexistencia.

Pollination success increases with plant diversity in high-Andean communities.

Pollinator-mediated plant-plant interactions have traditionally been viewed within the competition paradigm. However, facilitation via pollinator sharing might be the rule rather than the exception in harsh environments. Moreover, plant diversity could be playing a key role in fostering pollinator-mediated facilitation. Yet, the facilitative effect of plant diversity on pollination remains poorly understood, especially under natural conditions. By examining a total of 9371 stigmas of 88 species from nine high-Andean communities in NW Patagonia, we explored the prevalent sign of the relation between conspecific pollen receipt and heterospecific pollen diversity, and assessed whether the incidence of different outcomes varies with altitude and whether pollen receipt relates to plant diversity. Conspecific pollen receipt increased with heterospecific pollen diversity on stigmas. In all communities, species showed either positive or neutral but never negative relations between the number of heterospecific pollen donor species and conspecific pollen receipt. The incidence of species showing positive relations increased with altitude. Finally, stigmas collected from communities with more co-flowering species had richer heterospecific pollen loads and higher abundance of conspecific pollen grains. Our findings suggest that plant diversity enhances pollination success in high-Andean plant communities. This study emphasizes the importance of plant diversity in fostering indirect plant-plant facilitative interactions in alpine environments, which could promote species coexistence and biodiversity maintenance.

Negative impacts of dominance on bee communities: Does the influence of invasive honey bees differ from native bees?

Invasive species can reach high abundances and dominate native environments. One of the most impressive examples of ecological invasions is the spread of the African subspecies of the honey bee throughout the Americas, starting from its introduction in a single locality in Brazil. The invasive honey bee is expected to more negatively impact bee community abundance and diversity than native dominant species, but this has not been tested previously. We developed a comprehensive and systematic bee sampling scheme, using a protocol deploying 11,520 pan traps across regions and crops for three years in Brazil. We found that invasive honey bees are now the single most dominant bee species. Such dominance has not only negative consequences for abundance and species richness of native bees but also for overall bee abundance (i.e., strong "numerical" effects of honey bees). Contrary to expectations, honey bees did not have stronger negative impacts than other native bees achieving similar levels of dominance (i.e., lack of negative "identity" effects of honey bees). These effects were markedly consistent across crop species, seasons and years, and were independent from land-use effects. Dominance could be a proxy of bee community degradation and more generally of the severity of ecological invasions.

Intentional and unintentional selection during plant domestication: herbivore damage, plant defensive traits and nutritional quality of fruit and seed crops.

Greater susceptibility to herbivory can arise as an effect of crop domestication. One proposed explanation is that defenses decreased intentionally or unintentionally during the domestication process, but evidence for this remains elusive. An alternative but nonexclusive explanation is presumed selection for higher nutritional quality. We used a metaanalytical approach to examine susceptibility to herbivores in fruit and seed crops and their wild relatives. Our analyses provide novel insights into the mechanisms of increased susceptibility by evaluating whether it can be attributed to either a reduction in herbivore defensive traits, including direct/indirect and constitutive/inducible defenses, or an increase in the nutritional content of crops. The results confirm higher herbivory and lower levels of all types of defenses in crops compared to wild relatives, although indirect defenses were more affected than direct ones. Contrary to expectations, nutritional quality was lower in crops than in wild relatives, which may enhance biomass loss to herbivores if they increase consumption to meet nutritional requirements. Our findings represent an important advance in our understanding of how changes in defensive and nutritional traits following domestication could influence, in combination or individually, crop susceptibility to herbivore attacks.

Bees increase crop yield in an alleged pollinator-independent almond variety.

Wild pollinators are declining and the number of managed honey bee colonies is growing slower than agricultural demands for pollination. Because of these contrasting trends in pollinator demand and availability, breeding programs for many pollinator-dependent crops have focused on reducing the need for pollinators. Although numerous crop varieties are now available in the market with the label of pollinator-independent, the real dependence of these varieties on pollinators is mostly unknown. We evaluated the hypothesis of pollinator independence in the Independence almond variety, the fastest growing variety in California that is the main almond production region in the world. In this presumed pollinator-independent variety, we measured the effect of honey bees on fruit set, yield, and kernel nutritional quality at tree level. Fruit set was 60% higher in bee-pollinated than bee-isolated trees, which translated into a 20% increase in kernel yield. Despite its effect on almond production, there was no evidence that bee visitation affected almond nutritional quality. Based on these results, we recommend the use of bees, whether they are wild or managed, to maximize yield even in self-fertile almond varieties.

Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification.

The global increase in the proportion of land cultivated with pollinator-dependent crops implies increased reliance on pollination services. Yet agricultural practices themselves can profoundly affect pollinator supply and pollination. Extensive monocultures are associated with a limited pollinator supply and reduced pollination, whereas agricultural diversification can enhance both. Therefore, areas where agricultural diversity has increased, or at least been maintained, may better sustain high and more stable productivity of pollinator-dependent crops. Given that >80% of all crops depend, to varying extents, on insect pollination, a global increase in agricultural pollinator dependence over recent decades might have led to a concomitant increase in agricultural diversification. We evaluated whether an increase in the area of pollinator-dependent crops has indeed been associated with an increase in agricultural diversity, measured here as crop diversity, at the global, regional, and country scales for the period 1961-2016. Globally, results show a relatively weak and decelerating rise in agricultural diversity over time that was largely decoupled from the strong and continually increasing trend in agricultural dependency on pollinators. At regional and country levels, there was no consistent relationship between temporal changes in pollinator dependence and crop diversification. Instead, our results show heterogeneous responses in which increasing pollinator dependence for some countries and regions has been associated with either an increase or a decrease in agricultural diversity. Particularly worrisome is a rapid expansion of pollinator-dependent oilseed crops in several countries of the Americas and Asia that has resulted in a decrease in agricultural diversity. In these regions, reliance on pollinators is increasing, yet agricultural practices that undermine pollination services are expanding. Our analysis has thereby identified world regions of particular concern where environmentally damaging practices associated with large-scale, industrial agriculture threaten key ecosystem services that underlie productivity, in addition to other benefits provided by biodiversity.

The interplay between ovule number, pollination and resources as determinants of seed set in a modular plant.

BACKGROUND: A classical dichotomous perspective proposes that either pollination or plant resources limit seed production. However, ovule number could also be limiting when pollination results in complete ovule fertilization and there are more plant resources available than needed to develop seeds. Moreover, this dichotomous view assumes that all flowers of a plant have equal access to a shared pool of resources, although these are frequently compartmentalized within plant modules, for example, inflorescences. How ovule number, pollination and resources affect seed production in physiologically-compartmentalized rather than physiologically-integrated plants has yet to be explored. We used raspberry (Rubus idaeus) to address this question. METHODS: We first assessed if ovule number affected the fraction of ovules that develop into seed (i.e., seed set) and whether this effect related to the extent of physiological integration among flowers within plants. This was achieved by statistically testing predictions on the sign and level of plant organization (i.e., among flowers within inflorescences, among inflorescences within ramets, and among ramets) of the relation between ovule number and seed set given different degrees of physiological integration. We then explored whether the relation between ovule number and seed set was affected by plant age (used here as a surrogate of resource availability) and pollination intensity (open-pollination vs. exclusion). RESULTS: Within inflorescences, flowers with more ovules set a larger fraction of seeds. On the other hand, seed set at the inflorescence level was negatively related to the average number of ovules per flower. Seed set increased with ovule number and open-pollination, and decreased with ramet age. However, ovule number explained more variation in seed set than ramet age and pollination treatment. Ramet age affected the strength of the relation of seed set to ovule number, which was stronger in old than young ramets. Pollination did not alter the strength of this relation to any significant extent. DISCUSSION: Results reveal the importance of ovule number as an overriding factor affecting seed set. Within inflorescences, resources appear to be differentially allocated to developing fruits from flowers with many ovules. This is consistent with the fact that in the raspberry a large proportion of the carbon invested in fruit development is fixed by the inflorescence subtending leaf. Differential resource allocation to flowers with many ovules is not affected by pollinator exclusion, being stronger in resource-exhausted ramets. This suggests that the effects of pollen limitation and resource allocation are compartmentalized at the inflorescence level. Consequently, modular plants can be viewed as reproductive mosaics where either ovule number, pollination or resources limit the number of seeds set by different flowers, so that improvements in any of them could increase plant seed production.

The costs and benefits of pollinator dependence: empirically based simulations predict raspberry fruit quality.

Globally, agriculture increasingly depends on pollinators to produce many seed and fruit crops. However, what constitutes optimal pollination service for pollinator-dependent crops remains unanswered. We developed a simulation model to identify the optimal pollination service that maximizes fruit quality in crops. The model depicts the pollination (i.e., autonomous self-fertilization, pollen deposition) and post-pollination (i.e., pollen germination, and time from germination to ovule fertilization) processes leading to fruit and seed set and allows for negative flower-pollinator interactions, specifically pistil damage. We parameterized and validated the model based on empirical observations of commercial raspberry in western Argentina. To assess the effects of pollination intensity for fruit production, we conducted simulations over a range of visit number per flower by the two primary managed pollinators worldwide, Apis mellifera and Bombus terrestris. Simulations identified that ~15-35 visits per flower by A. mellifera or ~10-20 visits by B. terrestris provide adequate pollination and maximize raspberry fruit quality (i.e., estimated as the proportion of ovules that develop into drupelets). Visits in excess of these optima reduce simulated fruit quality, and flowers receiving >670 honey bee visits or >470 bumble bee visits would produce fruits of poorer quality than those receiving no bee visits. The simulations generated consistent, unbiased predictions of fruit quality for 12 raspberry fields. This model could be adapted easily to other animal-pollinated crops and used to guide efficient pollinator management in any agro-ecosystem.

An overlooked plant-parakeet mutualism counteracts human overharvesting on an endangered tree.

The exponential growth of the human population often causes the overexploitation of resources and disruption of ecological interactions. Here, we propose that the antagonist effect of humans on exploited species might be alleviated with the advent of a second predator species. We focused on the complex interactions between an endangered conifer (Araucaria araucana) and two seed exploiters: the Austral parakeet (Enicognathus ferrugineus) and human seed collectors. We tested the importance of partial seed consumption by parakeets as an escape from human seed harvesting. Although parakeets frequently ate whole seeds, a substantial proportion of the seeds found under trees were only partially eaten and avoided by human seed collectors. These seeds germinated at a similar proportion but faster than intact seeds under laboratory conditions. Our results revealed an overlooked mutualism between parakeets and an endangered tree. Incomplete seed eating by parakeets, plus selection against these eaten seeds by humans, may enhance regeneration possibilities for this conifer species subject to human seed collection, turning the scale of the antagonism-mutualism continuum to the mutualistic side. In this context, parakeets might be providing an important service in those forests subject to human harvesting by allowing a fraction of seeds to escape human predation.

Global decline of bumblebees is phylogenetically structured and inversely related to species range size and pathogen incidence.

Conservation biology can profit greatly from incorporating a phylogenetic perspective into analyses of patterns and drivers of species extinction risk. We applied such an approach to analyse patterns of bumblebee (Bombus) decline. We assembled a database representing approximately 43% of the circa 260 globally known species, which included species extinction risk assessments following the International Union fo Conservation of Nature Red List categories and criteria, and information on species traits presumably associated with bumblebee decline. We quantified the strength of phylogenetic signal in decline, range size, tongue length and parasite presence. Overall, about one-third of the assessed bumblebees are declining and declining species are not randomly distributed across the Bombus phylogeny. Susceptible species were over-represented in the subgenus Thoracobombus (approx. 64%) and under-represented in the subgenus Pyrobombus (approx. 6%). Phylogenetic logistic regressions revealed that species with small geographical ranges and those in which none of three internal parasites were reported (i.e. Crithidia bombi, Nosema spp. or Locustacarus buchneri) were particularly vulnerable. Bumblebee evolutionary history will be deeply eroded if most species from threatened clades, particularly those stemming from basal nodes, become finally extinct. The habitat of species with restricted distribution should be protected and the importance of pathogen tolerance/resistance as mechanisms to deal with pathogens needs urgent research.

The phylogenetic structure of plant-pollinator networks increases with habitat size and isolation.

Similarity among species in traits related to ecological interactions is frequently associated with common ancestry. Thus, closely related species usually interact with ecologically similar partners, which can be reinforced by diverse co-evolutionary processes. The effect of habitat fragmentation on the phylogenetic signal in interspecific interactions and correspondence between plant and animal phylogenies is, however, unknown. Here, we address to what extent phylogenetic signal and co-phylogenetic congruence of plant-animal interactions depend on habitat size and isolation by analysing the phylogenetic structure of 12 pollination webs from isolated Pampean hills. Phylogenetic signal in interspecific interactions differed among webs, being stronger for flower-visiting insects than plants. Phylogenetic signal and overall co-phylogenetic congruence increased independently with hill size and isolation. We propose that habitat fragmentation would erode the phylogenetic structure of interaction webs. A decrease in phylogenetic signal and co-phylogenetic correspondence in plant-pollinator interactions could be associated with less reliable mutualism and erratic co-evolutionary change.

Hot spots of mutualistic networks.

Incorporating interactions into a biogeographical framework may serve to understand how interactions and the services they provide are distributed in space. We begin by simulating the spatiotemporal dynamics of realistic mutualistic networks inhabiting spatial networks of habitat patches. We proceed by comparing the predicted patterns with the empirical results of a set of pollination networks in isolated hills of the Argentinian Pampas. We first find that one needs to sample up to five times as much area to record interactions as would be needed to sample the same proportion of species. Secondly, we find that peripheral patches have fewer interactions and harbour less nested networks - therefore potentially less resilient communities - compared to central patches. Our results highlight the important role played by the structure of dispersal routes on the spatial distribution of community patterns. This may help to understand the formation of biodiversity hot spots.

Node-by-node disassembly of a mutualistic interaction web driven by species introductions.

Interaction webs summarize the diverse interactions among species in communities. The addition or loss of particular species and the alteration of key interactions can lead to the disassembly of the entire interaction web, although the nontrophic effects of species loss on interaction webs are poorly understood. We took advantage of ongoing invasions by a suite of exotic species to examine their impact in terms of the disassembly of an interaction web in Patagonia, Argentina. We found that the reduction of one species (a host of a keystone mistletoe species) resulted in diverse indirect effects that led to the disassembly of an interaction web through the loss of the mistletoe, two key seed-dispersers (a marsupial and a bird), and a pollinator (hummingbird). Our results demonstrate that the gains and losses of species are both consequences and drivers of global change that can lead to underappreciated cascading coextinctions through the disruption of mutualisms.

Wild pollinators enhance fruit set of crops regardless of honey bee abundance.

The diversity and abundance of wild insect pollinators have declined in many agricultural landscapes. Whether such declines reduce crop yields, or are mitigated by managed pollinators such as honey bees, is unclear. We found universally positive associations of fruit set with flower visitation by wild insects in 41 crop systems worldwide. In contrast, fruit set increased significantly with flower visitation by honey bees in only 14% of the systems surveyed. Overall, wild insects pollinated crops more effectively; an increase in wild insect visitation enhanced fruit set by twice as much as an equivalent increase in honey bee visitation. Visitation by wild insects and honey bees promoted fruit set independently, so pollination by managed honey bees supplemented, rather than substituted for, pollination by wild insects. Our results suggest that new practices for integrated management of both honey bees and diverse wild insect assemblages will enhance global crop yields.