How does climate change impact social bees and bee sociality?

Climatic factors are known to shape the expression of social behaviours. Likewise, variation in social behaviour can dictate climate responses. Understanding interactions between climate and sociality is crucial for forecasting vulnerability and resilience to climate change across animal taxa. These interactions are particularly relevant for taxa like bees that exhibit a broad diversity of social states. An emerging body of literature aims to quantify bee responses to environmental change with respect to variation in key functional traits, including sociality. Additionally, decades of research on environmental drivers of social evolution may prove fruitful for predicting shifts in the costs and benefits of social strategies under climate change. In this review, we explore these findings to ask two interconnected questions: (a) how does sociality mediate vulnerability to climate change, and (b) how might climate change impact social organisation in bees? We highlight traits that intersect with bee sociality that may confer resilience to climate change (e.g. extended activity periods, diet breadth, behavioural thermoregulation) and we generate predictions about the impacts of climate change on the expression and distribution of social phenotypes in bees. The social evolutionary consequences of climate change will be complex and heterogeneous, depending on such factors as local climate and plasticity of social traits. Many contexts will see an increase in the frequency of eusocial nesting as warming temperatures accelerate development and expand the temporal window for rearing a worker brood. More broadly, climate-mediated shifts in the abiotic and biotic selective environments will alter the costs and benefits of social living in different contexts, with cascading impacts at the population, community and ecosystem levels.

Individual Variation in Male Pheromone Production in Xylocopa sonorina Correlates with size and Gland Color.

Sex pheromones are species-specific chemical signals that facilitate the location, identification, and selection of mating partners. These pheromones can vary between individuals, and act as signals of mate quality. Here, we investigate the variation of male pheromones in the mesosomal glands of the large carpenter bee Xylocopa sonorina, within a Northern California population. We tested the hypothesis that morphological traits are correlated with the observed variation in chemical blend composition of these bees. We also conducted behavioral assays to test whether these male pheromones act as long-range attractants to conspecifics. We found that larger males with darker mesosomal glands have a higher pheromone amount in their glands. Our analysis also suggests that this pheromone blend functions as a long-range attractant to both males and females. We show that both male body size and sexual maturation are important factors influencing pheromone abundance, and that this pheromone blend acts as a long-range attractant. We hypothesize that this recorded variation in male pheromone could be important for female choice.

Social conditions facilitate water conservation in a solitary bee.

Climatic stressors are important drivers in the evolution of social behavior. Social animals tend to thrive in harsh and unpredictable environments, yet the precise benefits driving these patterns are often unclear. Here, we explore water conservation in forced associations of a solitary bee (Melissodes tepidus timberlakei Cockerell, 1926) to test the hypothesis that grouping can generate synergistic physiological benefits in an incipient social context. Paired bees displayed mutual tolerance and experienced reduced water loss relative to singleton bees when exposed to acute low-humidity stress, with no change in activity levels. While the mechanism underlying these benefits remains unknown, social advantages like these can facilitate the evolution of cooperation among nonrelatives and offer important insights into the social consequences of climate change.

Incipiently social carpenter bees (Xylocopa) host distinctive gut bacterial communities and display geographical structure as revealed by full-length PacBio 16S rRNA sequencing.

The gut microbiota of bees affects nutrition, immunity and host fitness, yet the roles of diet, sociality and geographical variation in determining microbiome structure, including variant-level diversity and relatedness, remain poorly understood. Here, we use full-length 16S rRNA amplicon sequencing to compare the crop and gut microbiomes of two incipiently social carpenter bee species, Xylocopa sonorina and Xylocopa tabaniformis, from multiple geographical sites within each species' range. We found that Xylocopa species share a set of core taxa consisting of Bombilactobacillus, Bombiscardovia and Lactobacillus, found in >95% of all individual bees sampled, and Gilliamella and Apibacter were also detected in the gut of both species with high frequency. The crop bacterial community of X. sonorina comprised nearly entirely Apilactobacillus with occasionally abundant nectar bacteria. Despite sharing core taxa, Xylocopa species' microbiomes were distinguished by multiple bacterial lineages, including species-specific variants of core taxa. The use of long-read amplicons revealed otherwise cryptic species and population-level differentiation in core microbiome members, which was masked when a shorter fragment of the 16S rRNA (V4) was considered. Of the core taxa, Bombilactobacillus and Bombiscardovia exhibited differentiation in amplicon sequence variants among bee populations, but this was lacking in Lactobacillus, suggesting that some bacterial genera in the gut may be structured by different processes. We conclude that these Xylocopa species host a distinctive microbiome, similar to that of previously characterized social corbiculate apids, which suggests that further investigation to understand the evolution of the bee microbiome and its drivers is warranted.

Social consequences of energetically costly nest construction in a facultatively social bee.

Social groups form when the costs of breeding independently exceed fitness costs imposed by group living. The costs of independent breeding can often be energetic, especially for animals performing expensive behaviours, such as nest construction. To test the hypothesis that nesting costs can drive sociality by disincentivizing independent nest founding, we measured the energetics of nest construction and inheritance in a facultatively social carpenter bee (Xylocopa sonorina Smith), which bores tunnel nests in wood. We measured metabolic rates of bees excavating wood and used computerized tomography images of nesting logs to measure excavation volumes. From these data, we demonstrate costly energetic investments in nest excavation of a minimum 4.3 kJ per offspring provisioned, an expense equivalent to nearly 7 h of flight. This high, potentially prohibitive cost of nest founding may explain why females compete for existing nests rather than constructing new ones, often leading to the formation of social groups. Further, we found that nest inheritors varied considerably in their investment in nest renovation, with costs ranging more than 12-fold (from 7.08 to 89.1 kJ energy), probably reflecting differences in inherited nest quality. On average, renovation costs were lower than estimated new nest construction costs, with some nests providing major savings. These results suggest that females may join social groups to avoid steep energetic costs, but that the benefits of this strategy are not experienced equally.

The behavioral regulation of thirst, water collection and water storage in honey bee colonies.

This study investigated how a honey bee colony develops and quenches its collective thirst when it experiences hyperthermia of its broodnest. We found that a colony must strongly boost its water intake because evaporative cooling is critical to relieving broodnest hyperthermia, and that it must rapidly boost its water intake because a colony maintains only a small water reserve. We also clarified how a colony's water collectors know when to spring into action - by sensing either more frequent requests for fluid or greater personal thirst, or both. Finally, we found that the behavioral flexibility of a colony's water collectors enables them not only to satisfy their colony's current water needs but also to buffer their colony against future extreme water stresses by storing water in their crops and in their combs.

A critical number of workers in a honeybee colony triggers investment in reproduction.

Social insect colonies, like individual organisms, must decide as they develop how to allocate optimally their resources among survival, growth, and reproduction. Only when colonies reach a certain state do they switch from investing purely in survival and growth to investing also in reproduction. But how do worker bees within a colony detect that their colony has reached the state where it is adaptive to begin investing in reproduction? Previous work has shown that larger honeybee colonies invest more in reproduction (i.e., the production of drones and queens), however, the term 'larger' encompasses multiple colony parameters including number of adult workers, size of the nest, amount of brood, and size of the honey stores. These colony parameters were independently increased in this study to test which one(s) would increase a colony's investment in reproduction via males. This was assayed by measuring the construction of drone comb, the special type of comb in which drones are reared. Only an increase in the number of workers stimulated construction of drone comb. Colonies with over 4,000 workers began building drone comb, independent of the other colony parameters. These results show that attaining a critical number of workers is the key parameter for honeybee colonies to start to shift resources towards reproduction. These findings are relevant to other social systems in which a group's members must adjust their behavior as a function of the group's size.

Phenotypic divergence in an island bee population: Applying geometric morphometrics to discriminate population-level variation in wing venation.

Phenotypic divergence is an important consequence of restricted gene flow in insular populations. This divergence can be challenging to detect when it occurs through subtle shifts in morphological traits, particularly in traits with complex geometries, like insect wing venation. Here, we employed geometric morphometrics to assess the extent of variation in wing venation patterns across reproductively isolated populations of the social sweat bee, Halictus tripartitus. We examined wing morphology of specimens sampled from a reproductively isolated population of H. tripartitus on Santa Cruz Island (Channel Islands, Southern California). Our analysis revealed significant differentiation in wing venation in this island population relative to conspecific mainland populations. We additionally found that this population-level variation was less pronounced than the species-level variation in wing venation among three sympatric congeners native to the region, Halictus tripartitus, Halictus ligatus, and Halictus farinosus. Together, these results provide evidence for subtle phenotypic divergence in an island bee population. More broadly, these results emphasize the utility and potential of wing morphometrics for large-scale assessment of insect population structure.

Body mass and cuticular hydrocarbon profiles, but not queen number, underlie worker desiccation resistance in a facultatively polygynous harvester ant (Pogonomyrmex californicus).

As small-bodied terrestrial organisms, insects face severe desiccation risks in arid environments, and these risks are increasing under climate change. Here, we investigate the physiological, chemical, and behavioral mechanisms by which harvester ants, one of the most abundant arid-adapted insect groups, cope with desiccating environmental conditions. We aimed to understand how body size, cuticular hydrocarbon profiles, and queen number impact worker desiccation resistance in the facultatively polygynous harvester ant, Pogonomyrmex californicus. We measured survival at 0% humidity of field-collected worker ants sourced from three closely situated populations within a semi-arid region of southern California. These populations vary in queen number, with one population dominated by multi-queen colonies (primary polygyny), one population dominated by single-queen colonies, and one containing an even mix of single- and multi-queen colonies. We found no effect of population on worker survival in desiccation assays, suggesting that queen number does not influence colony desiccation resistance. Across populations, however, body mass and cuticular hydrocarbon profiles significantly predicted desiccation resistance. Larger-bodied workers survived longer in desiccation assays, emphasizing the importance of reduced surface area-to-volume ratios in maintaining water balance. Additionally, we observed a positive relationship between desiccation resistance and the abundance of n-alkanes, supporting previous work that has linked these high-melting point compounds to improved body water conservation. Together, these results contribute to an emerging model explaining the physiological mechanisms of desiccation resistance in insects.

Social Factors in Heat Survival: Multiqueen Desert Ant Colonies Have Higher and More Uniform Heat Tolerance.

AbstractInvestigations of thermally adaptive behavioral phenotypes are critical for both understanding climate as a selective force and predicting global species distributions under climate change conditions. Cooperative nest founding is a common strategy in harsh environments for many species and can enhance growth and competitive advantage, but whether this social strategy has direct effects on thermal tolerance was previously unknown. We examined the effects of alternative social strategies on thermal tolerance in a facultatively polygynous (multiqueen) desert ant, Pogonomyrmex californicus, asking whether and how queen number affects worker thermal tolerances. We established and reared lab colonies with one to four queens, then quantified all colony member heat tolerances (maximum critical temperature [CTmax]). Workers from colonies with more queens had higher and less variant CTmax. Our findings resemble weak link patterns, in which colony group thermal performance is improved by reducing frequencies of the most temperature-vulnerable individuals. Using ambient temperatures from our collection site, we show that multiqueen colonies have thermal tolerance distributions that enable increased midday foraging in hot desert environments. Our results suggest advantages to polygyny under climate change scenarios and raise the question of whether improved thermal tolerance is a factor that has enabled the success of polygyne species in other climatically extreme environments.

Cooperation among unrelated ant queens provides persistent growth and survival benefits during colony ontogeny.

The fitness consequences of cooperation can vary across an organism's lifespan. For non-kin groups, especially, social advantages must balance intrinsic costs of cooperating with non-relatives. In this study, we asked how challenging life history stages can promote stable, long-term alliances among unrelated ant queens. We reared single- and multi-queen colonies of the primary polygynous harvester ant, Pogonomyrmex californicus, from founding through the first ten months of colony growth, when groups face high mortality risks. We found that colonies founded by multiple, unrelated queens experienced significant survival and growth advantages that outlasted the colony founding period. Multi-queen colonies experienced lower mortality than single-queen colonies, and queens in groups experienced lower mortality than solitary queens. Further, multi-queen colonies produced workers at a faster rate than did single-queen colonies, even while experiencing lower per-queen worker production costs. Additionally, we characterized ontogenetic changes in the organization of labor, and observed increasing and decreasing task performance diversity by workers and queens, respectively, as colonies grew. This dynamic task allocation likely reflects a response to the changing role of queens as they are increasingly able to delegate risky and costly tasks to an expanding workforce. Faster worker production in multi-queen colonies may beneficially accelerate this behavioral transition from a vulnerable parent-offspring group to a stable, growing colony. These combined benefits of cooperation may facilitate the retention of multiple unrelated queens in mature colonies despite direct fitness costs, providing insight into the evolutionary drivers of stable associations between unrelated individuals.