skip to main content


Title: Developmental transcriptomes predict adult social behaviours in the socially flexible sweat bee, Lasioglossum baleicum
Abstract

Natural variation can provide important insights into the genetic and environmental factors that shape social behaviour and its evolution. The sweat bee,Lasioglossum baleicum, is a socially flexible bee capable of producing both solitary and eusocial nests. We demonstrate that within a single nesting aggregation, soil temperatures are a strong predictor of the social structure of nests. Sites with warmer temperatures in the spring have a higher frequency of social nests than cooler sites, perhaps because warmer temperatures provide a longer reproductive window for those nests. To identify the molecular correlates of this behavioural variation, we generated a de novo genome assembly forL. baleicum, and we used transcriptomic profiling to compare adults and developing offspring from eusocial and solitary nests. We find that adult, reproductive females have similar expression profiles regardless of social structure in the nest, but that there are strong differences between reproductive females and workers from social nests. We also find substantial differences in the transcriptomic profiles of stage‐matched pupae from warmer, social‐biased sites compared to cooler, solitary‐biased sites. These transcriptional differences are strongly predictive of adult reproductive state, suggesting that the developmental environment may set the stage for adult behaviours inL. baleicum. Together, our results help to characterize the molecular mechanisms shaping variation in social behaviour and highlight a potential role of environmental tuning during development as a factor shaping adult behaviour and physiology in this socially flexible bee.

 
more » « less
NSF-PAR ID:
10481887
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
ISSN:
0962-1083
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Bumble bee queens initiate nests solitarily and transition to living socially once they successfully rear their first cohort of offspring. Bumble bees are disproportionately important for early season pollination, and many populations are experiencing dramatic declines. In this system, the onset of the social stage is critical for nest survival, yet the mechanisms that facilitate this transition remain understudied. Further, the majority of conservation efforts target the social stage of the bumble bee life cycle and do not address the solitary founding stage. We experimentally manipulated the timing of worker emergence in young nests of bumble bee (Bombus impatiens) queens to determine whether and how queen fecundity and survival are impacted by the emergence of workers in the nest. We found that queens with workers added to the nest exhibit increased ovary activation, accelerated egg laying, elevated juvenile hormone (JH) titres and also lower mortality relative to solitary queens. We also show that JH is more strongly impacted by the social environment than associated with queen reproductive state, suggesting that this key regulator of insect reproduction has expanded its function in bumble bees to also influence social organization. We further demonstrate that these effects are independent of queen social history, suggesting that this underlying mechanism promoting queen fecundity is reversible and short lived. Synchronization between queen reproductive status and emergence of workers in the nest may ultimately increase the likelihood of early nesting success in social systems with solitary nest founding. Given that bumble bee workers regulate queen physiology as we have demonstrated, the timing of early worker emergence in the nest likely impacts queen fitness, colony developmental trajectories and ultimately nesting success. Collectively, our findings underline the importance of conservation interventions for bumble bees that support the early nesting period and facilitate the production and maintenance of workers in young nests 
    more » « less
  2. Abstract

    Tool‐using primates often show sex differences in both the frequency and efficiency of tool use. In species with sex‐biased dispersal, such within‐group variation likely shapes patterns of cultural transmission of tool‐use traditions between groups. On the Panamanian islands of Jicarón and Coiba, a population of white‐faced capuchins (Cebus capucinus imitator)—some of which engage in habitual stone tool use—provide an opportunity to test hypotheses about why such sex‐biases arise. On Jicarón, we have only observed males engaging in stone tool use, whereas on Coiba, both sexes are known to use tools. Using 5 years of camera trap data, we provide evidence that this variation likely reflects a sex difference in tool use rather than a sampling artifact, and then test hypotheses about the factors driving this pattern. Differences in physical ability or risk‐aversion, and competition over access to anvils do not account for the sex‐differences in tool‐use we observe. Our data show that adult females are physically capable of stone tool use: adult females on Coiba and juveniles on Jicarón smaller than adult females regularly engage in tool use. Females also have ample opportunity to use tools: the sexes are equally terrestrial, and competition over anvils is low. Finally, females rarely scrounge on left‐over food items either during or after tool‐using events, suggesting they are not being provisioned by males. Although it remains unclear why adult white‐faced capuchin females on Jicarón do not use stone‐tools, our results illustrate that such sex biases in socially learned behaviors can arise even in the absence of obvious physical, environmental, and social constraints. This suggests that a much more nuanced understanding of the differences in social structure, diet, and dispersal patterns are needed to explain why sex‐biases in tool use arise in some populations but not in others.

     
    more » « less
  3. Abstract

    Many social species show variation in their social structure in response to different environmental conditions. For example, colonies of the yellowjacket waspVespula squamosaare typically headed by a single reproductive queen and survive for only a single season. However, in warmer climates,V. squamosacolonies sometimes persist for multiple years and can grow to extremely large size. We used genetic markers to understand patterns of reproduction and recruitment within these perennial colonies. We genotypedV. squamosaworkers, pre‐reproductive queens, and males from perennial colonies in the southeastern United States at 10 polymorphic microsatellite loci and one mitochondrial DNA locus. We found thatV. squamosafrom perennial nests were produced by multiple reproductives, in contrast to typical annual colonies. Relatedness of nestmates from perennial colonies was significantly lower than relatedness of nestmates from annual colonies. Our analyses of mitochondrial DNA indicated that mostV. squamosaperennial colonies represented semiclosed systems whereby all individuals belonged to a single matriline despite the presence of multiple reproductive females. However, new queens recruited into perennial colonies apparently mated with non‐nestmate males. Notably, perennial and annual colonies did not show significant genetic differences, supporting the hypothesis that perennial colony formation represents an instance of social plasticity. Overall, our results indicate that perennialV. squamosacolonies show substantial changes to their social biology compared to typical annual colonies and demonstrate variation in social behaviors in highly social species.

     
    more » « less
  4. Abstract The temperature of the nest influences fitness in cavity-nesting bees. Females may choose nest cavities that mitigate their offspring’s exposure to stressful temperatures. This study aims to understand how cavity temperature impacts the nesting preference of the solitary bee Megachile rotundata (Fabricius) under field conditions. We designed and 3D printed nest boxes that measured the temperatures of 432 cavities. Nest boxes were four-sided with cavity entrances facing northeast, northwest, southeast, and southwest. Nest boxes were placed along an alfalfa field in Fargo, ND and were observed daily for completed nests. Our study found that cavity temperature varied by direction the cavity faced and by the position of the cavity within the nest box. The southwest sides recorded the highest maximum temperatures while the northeast sides recorded the lowest maximum temperatures. Nesting females filled cavities on the north-facing sides faster than cavities on the south-facing sides. The bees preferred to nest in cavities with lower average temperatures during foraging hours, and cavities that faced to the north. The direction the cavity faced was associated with the number of offspring per nest. The southwest-facing cavities had fewer offspring than nests on the northeast side. Our study indicates that the nesting box acts as a microclimate, with temperature varying by position and direction of the cavity. Variation in cavity temperature affected where females chose to nest, but not their reproductive investment. 
    more » « less
  5. Abstract

    Migratory, long‐lived animals are an important focus for life‐history theory because they manifest extreme trade‐offs in life‐history traits: delayed maturity, low fecundity, variable recruitment rates, long generation times, and vital rates that respond to variation across environments. Galapagos tortoises are an iconic example: they are long‐lived, migrate seasonally, face multiple anthropogenic threats, and have cryptic early life‐history stages for which vital rates are unknown. From 2012 to 2021, we studied the reproductive ecology of two species of Galapagos tortoises (Chelonoidis porteriandC. donfaustoi) along elevation gradients that coincided with substantial changes in climate and vegetation productivity. Specifically, we (1) measured the body and reproductive condition of 166 adult females, (2) tracked the movements of 33 adult females using global positioning system telemetry, and monitored their body condition seasonally, (3) recorded nest temperatures, clutch characteristics, and egg survival from 107 nests, and (4) used radiotelemetry to monitor growth, survival, and movements of 104 hatchlings. We also monitored temperature and rainfall from field sites, and remotely sensed primary productivity along the elevation gradient. Our study showed that environmental variability, mediated by elevation, influenced vital rates of giant tortoises, specifically egg production by adult females and juvenile recruitment. Adult females were either elevational migrants or year‐round lowland residents. Migrants had higher body condition than residents, and body condition was positively correlated with the probability of being gravid. Nests occurred in the hottest, driest parts of the tortoise's range, between 6 and 165 m elevation. Clutch size increased with elevation, whereas egg survival decreased. Hatchling survival and growth were highest at intermediate elevations. Hatchlings dispersed rapidly to 100–750 m from their nests before becoming sedentary (ranging over <0.2 ha). Predicted future climates may impact the relationships between elevation and vital rates of Galapagos tortoises and other species living across elevation gradients. Resilience will be maximized by ensuring the connectivity of foraging and reproductive areas within the current and possible future elevational ranges of these species.

     
    more » « less