Division of labour within social groups and the interspecific relationships within mutualisms have traditionally been treated as separate research areas. In this opinion, we align terminologies and concepts between the two fields, by comparing within-group division of labour to the outsourcing of functions in mutualisms. Division of labour and interspecific outsourcing share fundamental similarities. Both are built from specialization of some individuals within the relationship on tasks or functions required for survival, growth and reproduction. Both also generate variable fitness outcomes. A key difference is that mutualisms generally generate direct fitness gain, while benefits from cooperative sociality often accrue from a mix of direct and indirect fitness. Additionally, the levels of physical and physiological specialization within many mutualisms expand far beyond the levels of differentiation seen in cooperative social groups, with the exception of reproductive division of labour. The consideration of between-species outsourcing in the context of division of labour allows expansion of our understanding of both fields and beyond, to consider general principles as drivers of division of labour, and role differences more broadly across levels of complexity.This article is part of the theme issue 'Division of labour as key driver of social evolution'.

Many insects damage leaves, a phenomenon that is foundational to their impacts on terrestrial ecosystems. Leaf traits, including chemistry, shape these interactions. In turn, leaf-surface (phylloplane) microbes can act directly or in concert with leaf chemistry to influence leaf choice, especially by insects whose reproductive success is tied to prolonged contact with leaf surfaces. Leafcutter bees (Megachile spp.) cut disks from leaves to line their nests, with leaves and their associated microbes forming the environment in which bees' offspring develop. We hypothesized that phylloplane microbial communities act in concert with leaf chemistry to mediate interactions between the leafcutter bee M. lippiae and the plants they cut. We surveyed phylloplane communities on rose (Rosa × hybrida, Rosaceae) leaflets that were cut versus not cut by wild M. lippiae. Microbial communities differed between cut and non-cut leaflets, with Aspergillus spp. overrepresented on cut leaflets, and Alternaria sp. and Bacillus sp. overrepresented on non-cut leaflets. Then, we inoculated rose leaves in the field to test the effect of these microbial taxa on cutting. When inoculated onto rose leaves, Alternaria and Bacillus had no effect on cutting, but Aspergillus resulted in twice as many cuts as on sham-inoculated leaves. To test whether Aspergillus could protect bee nests against pathogens, we grew Aspergillus with two pathogenic fungi: the generalist insect pathogen Beauveria bassiania and three strains of Ascosphaera that cause chalkbrood disease in bee larvae. Aspergillus did not inhibit the growth of Beauveria, but it markedly slowed the growth of Ascosphaera. To clarify whether these phylloplane microbes reflect differences in leaf chemistry or are instead independent cues that influence leaf cutting, we used liquid chromatography-mass spectroscopy to characterize the metabolome of cut and non-cut leaflets. Chemistry did not differ between cut and non-cut leaflets, nor did it vary as a function of microbial community composition. Our results suggest that Aspergillus, a common member of rose phylloplane communities, mediates interactions between leafcutter bees and roses, potentially affecting the fitness of both partners. This study reveals a previously unexplored role for phylloplane microbes in plant-insect associations.

Mutualistic interactions are biological markets in which different species exchange commodities to mutual benefit. Mutualisms are, however, susceptible to exploitation, with some individuals taking without reciprocating. While it is generally assumed that exploiters will inflict fitness costs, evidence for such costs is mixed and difficult to generalize due to their context-dependent nature. Animal-pollinated flowers are commonly exploited by larcenists, non-pollinating animals that consume floral rewards often without transferring pollen. The impacts of larcenists on plant reproduction vary widely, suggesting they inflict differing costs on plants, but which types of floral larceny are most and least costly, and why, has received little attention. We employed a meta-analytical approach to explore the effects of flower larceny on nectar traits, pollinator visitation, and plant reproduction. We focused on the effects of two contrasting forms of larceny: primary nectar robbing-nectar consumption through holes constructed in the corolla rather than entering flowers legitimately-and nectar theft-nectar consumption by entering flowers but with no pollen transfer. We found that both robbing and theft had negative impacts on nectar quantity and quality, but that only theft negatively affected pollinator visitation rates. Similarly, robbers had no impact on either female or male reproductive success, whereas thieves consistently reduced both male and female reproductive success. These effects were not associated with plant mating systems nor with the identities of robbers and effective pollinators, challenging previous generalizations. This study provides a comprehensive evaluation of larcenists' costs to animal-pollinated plants, revealing that nectar theft is more detrimental to plant reproduction than nectar robbing. These results enhance our understanding of the intricate dynamics of mutualism exploitation in ecological and evolutionary contexts.

The literature on domestication commonly calls the association between human domesticators and their plant and animal domesticates mutualistic, yet this designation is rarely examined critically. Here, we assess its validity based on the long-accepted ecological definition of mutualism and current evidence for origins, subsequent evolution, and present features of domesticator-domesticate interactions. We argue that it is difficult to wholly align these associations with standard concepts of mutualism. Instead, domesticator-domesticate interactions vary across domestication pathways and have changed throughout domestication timelines, spanning antagonism to commensalism to mutualism. We argue that the later stages of domestication in some intensively domesticated species form exploitative rather than mutualistic interactions. Moving away from conceptualizing domestication as mutualistic raises new questions regarding its ecology and evolution.

The sacred datura plant (Solanales: Solanaceae: Datura wrightii ) has been used to study plant–herbivore interactions for decades. The wealth of information that has resulted leads it to have potential as a model system for studying the ecological and evolutionary genomics of these interactions. We present a de novo Datura wrightii genome assembled using PacBio HiFi long-reads. Our assembly is highly complete and contiguous (N50 = 179Mb, BUSCO Complete = 97.6%). We successfully detected a previously documented ancient whole genome duplication using our assembly and have classified the gene duplication history that generated its coding sequence content. We use it as the basis for a genome-guided differential expression analysis to identify the induced responses of this plant to one of its specialized herbivores (Coleoptera: Chrysomelidae: Lema daturaphila ). We find over 3000 differentially expressed genes associated with herbivory and that elevated expression levels of over 200 genes last for several days. We also combined our analyses to determine the role that different gene duplication categories have played in the evolution of Datura -herbivore interactions. We find that tandem duplications have expanded multiple functional groups of herbivore responsive genes with defensive functions, including UGT-glycosyltranserases, oxidoreductase enzymes, and peptidase inhibitors. Overall, our results expand our knowledge of herbivore-induced plant transcriptional responses and the evolutionary history of the underlying herbivore-response genes.

The Bulletin of the Ecological Society of America is the official record of business of the Ecological Society of America, publishing non-refereed articles that cover ecological events, news and reports.

Floral nectar contains microbes that can influence nectar chemistry and pollinator visitation, and these microbial communities can be affected by pollinators in turn. Some flowers are also visited by nectar robbers, which feed on nectar through holes cut in floral tissue. If nectar robbers alter nectar microbial communities, they might have unexpected impacts on pollinator visitation. We investigated whether robbing could affect nectar microbial communities directly, by introducing microbes, or indirectly, by triggering a plant response to floral damage. We applied four treatments to flowers of Tecoma x "Orange Jubilee" (Bignoniaceae) in an arboretum setting: flowers were (1) covered to exclude all visitors; (2) available to both pollinators and nectar robbers and robbed naturally by carpenter bees; (3) available to pollinators only but cut at the base to simulate nectar robbing damage; or (4) available to pollinators only. We found that nectar in flowers accessible to any visitors was more likely to contain culturable microbes than flowers from which visitors were excluded. Microbial community composition and beta diversity were similar across treatments. Among flowers containing culturable microbes, flowers available to pollinators and nectar robbers had higher microbial abundance than flowers with simulated robbing, but there were no differences between flowers available to pollinators and robbers and unwounded flowers from which robbers were excluded. Overall, our results suggest that floral damage can affect some features of nectar microbial communities, but specific effects of nectar robbing are limited compared with the influence of visitation in general. This study experimentally tested whether nectar robbers and pollinators differ in their effects on nectar microbial communities of Tecoma x "Orange Jubilee" and whether any differences are due specifically to floral damage caused by robbing. Simulated robbing damage (but not natural robbing) decreased microbial abundance, relative to flowers from which robbers were excluded. Nectar microbial communities were otherwise similar in robbed and unrobbed flowers, and we found much greater differences between flowers that were unvisited versus flowers that received any kind of visit (robber or pollinator).image

The assembly of genomes from pooled samples of genetically heterogenous samples of conspecifics remains challenging. In this study, we show that high-quality genome assemblies can be produced from samples of multiple wild-caught individuals. We sequenced DNA extracted from a pooled sample of conspecific herbivorous insects (Hemiptera: Miridae: Tupiocoris notatus) acquired from a greenhouse infestation in Tucson, Arizona (in the range of 30-100 individuals; 0.5 mL tissue by volume) using PacBio highly accurate long reads (HiFi). The initial assembly contained multiple haplotigs (>85% BUSCOs duplicated), but duplicate contigs could be easily purged to reveal a highly complete assembly (95.6% BUSCO, 4.4% duplicated) that is highly contiguous by short-read assembly standards (N-50 = 675 kb; Largest contig = 4.3 Mb). We then used our assembly as the basis for a genome-guided differential expression study of host plant-specific transcriptional responses. We found thousands of genes (N = 4982) to be differentially expressed between our new data from individuals feeding on Datura wrightii (Solanaceae) and existing RNA-seq data from Nicotiana attenuata (Solanaceae)-fed individuals. We identified many of these genes as previously documented detoxification genes such as glutathione-S-transferases, cytochrome P450s, and UDP-glucosyltransferases. Together our results show that long-read sequencing of pooled samples can provide a cost-effective genome assembly option for small insects and can provide insights into the genetic mechanisms underlying interactions between plants and herbivorous pests.

The ant communities within Biosphere 2, a massive, enclosed set of human-constructed habitats in southern Arizona, had not been examined in >20 yr. Throughout 2018, we conducted five ant surveys within and around Biosphere 2 to determine the current species composition and to determine whether species within the facility are establishing in the surrounding native habitat. As in previous surveys, we found exceedingly high numbers of Paratrechina longicornis, an invasive ant species, within every Biosphere 2 "biome" that we examined. We also found it to be present in the habitat surrounding the structure. How species that thrive in disturbed ecosystems infiltrate and affect native ecosystems is critical to understand, especially for systems intended to be sealed, such as Biosphere 2.

Plant species bearing extrafloral nectaries (EFNs) may indirectly influence other plant species by sharing protective ants, potentially altering plant herbivory levels. However, the propagation of indirect effects in this type of mutualism has seldom been investigated. We investigated indirect effects via ant sharing among twenty-one EFN-bearing plant species of the tribe Bignonieae distributed on 28 plots in the central Brazilian Amazon. Using an ecological network index that quantifies potential indirect effects among plant species via ant sharing, we distinguished plant species that could most strongly affect and most strongly be affected by other species via shared dominant and subordinate ant species. These Bignonieae species differ markedly in attractiveness to ants, and we investigated how these differences influenced the indirect effects between plant species. We also tested whether plant species with a higher potential to influence ant visitation to other plants experienced less herbivory due to attraction of more aggressive/dominant ants. We found that the most attractive plant species (here termed the promoter species) had the highest potential to indirectly affect ant visitation to less attractive plant species (here termed the receptor species) in the community, mainly via changes in attraction of dominant ant species. However, the potential indirect effects among plants did not translate into herbivory patterns. We also found that ant attendance and herbivory did not differ among promoter species, their neighbours, and non-neighbouring plants. We conclude that, unlike patterns found in studies investigating indirect effects in other mutualisms involving plants (e.g., pollination), the consequences of indirect effects among plant species are limited in this ant-plant network. This pattern could be explained by generally low herbivory levels and the small foraging areas of shared ant defenders. Indirect interactions and their effects between plant species that share protective ants appear in this system to confer limited costs and benefits.

Primary nectar-robbers feed through holes they make in flowers, often bypassing the plant’s reproductive organs in the process. In many robbed plants, multiple holes are made in a single flower. Why a flower should be robbed repeatedly is difficult to understand: a hole signals that a nectar forager has already fed, which would seem likely to predict low rewards. We tested three explanations for this pattern in Corydalis caseana (Fumariaceae), a bumble bee pollinated and robbed plant: (1) multiple holes appear only after all flowers have been robbed once; (2) individual foragers make multiple holes during single visits; and (3) it is more profitable for bees to rob older flowers, even if they have already been robbed. We tested these hypotheses from 2014 to 2016 in a Colorado, USA population using data on robbing rates over time, floral longevity, nectar accumulation in visited and unvisited flowers, and the accumulation of robbing holes across the life of flowers. Multiple holes were already appearing when two-thirds of flowers still lacked a single hole, allowing us to reject the first hypothesis. The second hypothesis cannot offer a full explanation for multiple robbing holes because 35% of additional holes appeared in flowers one or more days after the first hole was made. Repeated sampling of bagged and exposed inflorescences revealed that flowers filled at a constant rate and refilled completely after being drained. Consequently, young flowers are of consistently low value to foragers compared to older flowers even if they had previously been robbed, consistent with the third hypothesis. While further studies are needed, these results offer a simple explanation for the paradoxical clustering of nectar-robbing damage in this and possibly other plant species.

There has long been a fundamental divide in the study of cooperation: researchers focus either on cooperation within species, including but not limited to sociality, or else on cooperation between species, commonly termed mutualism. Here, we explore the ecologically and evolutionarily significant ways in which within- and between-species cooperation interact. We highlight two primary cross-linkages. First, cooperation of one type can change the context in which cooperation of the other type functions, and thus potentially its outcome. We delineate three possibilities: (i) within-species cooperation modulates benefits for a heterospecific partner; (ii) between-species cooperation affects the dynamics of within-species cooperation; and (iii) both processes take place interactively. The second type of cross-linkage emerges when resources or services that cooperation makes available are obtainable either from members of the same species or from different species. This brings cooperation at the two levels into direct interaction, to some extent obscuring the distinction between them. We expand on these intersections between within- and between-species cooperation in a diversity of taxa and interaction types. These interactions have the potential to weave together social networks and trophic dynamics, contributing to the structure and functioning of ecological communities in ways that are just beginning to be explored. This article is part of the theme issue ‘Connected interactions: enriching food web research by spatial and social interactions’.

Interactions between plants and herbivores are central in most ecosystems, but their strength is highly variable. The amount of variability within a system is thought to influence most aspects of plant-herbivore biology, from ecological stability to plant defense evolution. Our understanding of what influences variability, however, is limited by sparse data. We collected standardized surveys of herbivory for 503 plant species at 790 sites across 116° of latitude. With these data, we show that within-population variability in herbivory increases with latitude, decreases with plant size, and is phylogenetically structured. Differences in the magnitude of variability are thus central to how plant-herbivore biology varies across macroscale gradients. We argue that increased focus on interaction variability will advance understanding of patterns of life on Earth.

Photo 1. Extrafloral nectar production by extrafloral nectaries located in vegetative parts (base of leaf petiole) in Qualea multiflora. Extrafloral nectar is mainly produced early in the morning (A–C) and at night (D) attracting mutualists ants (Photo 3) that protect the host plant against herbivore attack. Photo credit: Eduardo Calixto. Photo 2. Inflorescence of Qualea multiflora (A), which also bears extrafloral nectaries at the base of each flower bud (B). When extrafloral nectaries on leaves are active, which occurs on newly flushed leaves, extrafloral nectaries on inflorescences are not. When leaves are fully expanded, foliar extrafloral nectaries cease their activity, and inflorescence extrafloral nectaries start to produce nectar. Photo credit: Denise Lange. Photo 3. Ectatomma tuberculatum ant collecting nectar from Qualea multiflora. Note the drop of extrafloral nectar between its mandibles. Photo credit: Denise Lange. These photographs illustrate the article “Time course of inducibility of indirect responses in an ant-defended plant” by Eduardo S. Calixto, Kleber Del-Claro, Denise Lange, and Judith Bronstein published in Ecology. https://doi.org/10.1002/ECY.4029

Predicting the impacts of global warming on mutualisms poses a significant challenge given the functional and life history differences that usually exist among interacting species. However, this is a critical endeavour since virtually all species on Earth depend on other species for survival and/or reproduction. The field of thermal ecology can provide physiological and mechanistic insights, as well as quantitative tools, for addressing this challenge. Here, we develop a conceptual and quantitative framework that connects thermal physiology to species' traits, species' traits to interacting mutualists' traits and interacting traits to the mutualism. We first identify the functioning of reciprocal mutualism-relevant traits in diverse systems as the key temperature-dependent mechanisms driving the interaction. We then develop metrics that measure the thermal performance of interacting mutualists' traits and that approximate the thermal performance of the mutualism itself. This integrated approach allows us to additionally examine how warming might interact with resource/nutrient availability and affect mutualistic species' associations across space and time. We offer this framework as a synthesis of convergent and critical issues in mutualism science in a changing world, and as a baseline to which other ecological complexities and scales might be added.

Understanding mechanisms that generate range limits is central to knowing why species are found where they are and how they will respond to environmental change. There is growing awareness that biotic interactions play an important role in generating range limits. However, current theory and data overwhelmingly focus on abiotic drivers and antagonistic interactions. Here we explore the effect that mutualists have on their partner's range limits: the geographic "footprint" of mutualism. This footprint arises from two general processes: modification of a partner's niche through environment-dependent fitness effects and, for a subset of mutualisms, dispersal opportunities that lead suitable habitats to be filled. We developed a conceptual framework that organizes different footprints of mutualism and the underlying mechanisms that shape them, and evaluated supporting empirical evidence from the primary literature. In the available literature, we found that the fitness benefits and dispersal opportunities provided by mutualism can extend species' ranges; conversely, the absence of mutualism can constrain species from otherwise suitable regions of their range. Most studies found that the footprint of mutualism is driven by changes in the frequency of mutualist partners from range core to range edge, whereas fewer found changes in interaction outcomes, the diversity of partners, or varying sensitivities of fitness to the effects of mutualists. We discuss these findings with respect to specialization, dependence, and intimacy of mutualism. Much remains unknown about the geographic footprint of mutualisms, leaving fruitful areas for future work. A particularly important future direction is to explore the role of mutualism during range shifts under global change, including the promotion of shifts at leading edges and persistence at trailing edges.

Plants have evolved inducible defenses that allow them to minimize costs associated with the production of constitutive defenses when herbivores are not present. However, as a consequence, some plants might experience a period of vulnerability between damage and the onset of defense and/or between the cessation of damage and relaxation of defense. Few studies have examined the time course in the inducible protective mutualism between ants and extrafloral nectary (EFN)-bearing plants. None has compared the inducibility of EFNs on vegetative versus reproductive parts or in response to different levels of herbivore damage. Here, we disentangle the inducibility process by evaluating extrafloral nectar production and ant attendance over time, the time course of inducibility on different plant parts, and the time course of inducibility in response to different levels of foliar damage in a Brazilian tree, Qualea multiflora (Vochysiaceae). Using simulated herbivory on leaves and flowers, we found that (a) the production of extrafloral nectar from foliar and floral EFNs, as well as ant attendance, exhibited a lag between the moment of damage and the peak of response, followed by a response peak (usually 24 h after damage) at which the defense remains at its maximum level, then declines to prestimulus levels; (b) the time course of inducibility and the peak activity did not differ between EFNs located in vegetative versus reproductive parts, except for sugar concentration, which was higher in EFNs on vegetative parts; and (c) the time course of inducibility of foliar EFNs depended on damage level. Although considered a cost-saving strategy, inducible defenses can be disadvantageous since they can leave plants vulnerable to attack for extended periods. Our results illuminate the dynamics of the induced response and the underlying mechanisms that might mediate it, ultimately providing new insights into defense strategies employed by plants.

Within-species variation in pollinator behavior is widely observed, but its causes have been minimally investigated. Pollinator sex is associated with large differences in behavior that may lead to predictable differences in flower foraging, but this expectation has not been explicitly tested. We investigate sex-associated differences in nectar-foraging behavior of the hawkmoth Hyles lineata, using pollen on the proboscis as a proxy for flower visitation. We tested two predictions emerging from the literature: (1) the sexes differ in the flower species they visit, (2) females are more specialized in flower choice. We also examined potential drivers underlying these predictions by performing field and laboratory experiments to test whether males (3) switch among flower species more frequently, or (4) fly farther and therefore encounter more species than females. Consistent with prediction (1), pollen load composition differed between the sexes, indicative of visitation differences. Contrary to prediction (2), females consistently carried more species-rich pollen loads than males. (3) Both sexes switched between flower species at similar rates, suggesting that differences in floral fidelity are unlikely to explain why females are less specialized than males. (4) Males flew longer distances than females; coupled with larger between-site differences in pollen composition for females, this result suggests that sex differences in mobility influence foraging, and that females may forage more frequently and in smaller areas than males. Together, our results demonstrate that sex-associated foraging differences can be large and consistent over time, and highlight the importance of sex as a driver of variation in pollinator behavior.

1. Precise pollen placement on floral visitors can improve pollen transfer, but in many plant species, pollen is deposited onto the flexible proboscises of long‐tongued insects. These proboscises are curled and uncurled between floral visits, potentially causing pollen to be lost or displaced. Rates of pollen movement and loss resulting from proboscis curling, and hence the potential quality of long‐tongued insects as pollinators, are unknown.2. Here, pollen loss and movement on the proboscises of Manduca sexta (Sphingidae) hawkmoths was experimentally measured. It was predicted that (i) proboscis curling causes pollen loss; (ii) pollen that is not lost is displaced from its deposition site; and (iii) repeated curls result in more displacement. Pollen from Datura wrightii, an important nectar plant for M. sexta, was placed distal to the knee bend on M. sexta proboscises, and the number and location of grains was recorded after proboscis curls.3. Consistent with the hypotheses, proboscis curling caused significant pollen loss. (i) A single curl resulted in the loss of almost 75% of the pollen from the placement site; after repeated curling, 98% of grains were lost from this site. (ii) A single curl was also sufficient to displace pollen across all surfaces of the proboscis, but (iii) further curling did not affect its distribution across surfaces.4. Together, these results suggest that precise pollen placement on the proboscises of hawkmoths would be unlikely to increase pollen transfer success. Strategies by which flowering plants might mitigate the effects of pollen loss from visitors with flexible pollen‐pickup structures are discussed.