Sequential Social Experiences Interact to Modulate Aggression but Not Brain Gene Expression in the Honey Bee (\u3cem\u3eApis mellifera\u3c/em\u3e)

Background: In highly structured societies, individuals behave flexibly and cooperatively in order to achieve a particular group-level outcome. However, even in social species, environmental inputs can have long lasting effects on individual behavior, and variable experiences can even result in consistent individual differences and constrained behavioral flexibility. Despite the fact that such constraints on behavior could have implications for behavioral optimization at the social group level, few studies have explored how social experiences accumulate over time, and the mechanistic basis of these effects. In the current study, I evaluate how sequential social experiences affect individual and group level aggressive phenotypes, and individual brain gene expression, in the highly social honey bee (Apis mellifera). To do this, I combine a whole colony chronic predator disturbance treatment with a lab-based manipulation of social group composition. Results: Compared to the undisturbed control, chronically disturbed individuals show lower aggression levels overall, but also enhanced behavioral flexibility in the second, lab-based social context. Disturbed bees display aggression levels that decline with increasing numbers of more aggressive, undisturbed group members. However, group level aggressive phenotypes are similar regardless of the behavioral tendencies of the individuals that make up the group, suggesting a combination of underlying behavioral tendency and negative social feedback influences the aggressive behaviors displayed, particularly in the case of disturbed individuals. An analysis of brain gene expression showed that aggression related biomarker genes reflect an individual’s disturbance history, but not subsequent social group experience or behavioral outcomes. Conclusions: In highly social animals with collective behavioral phenotypes, social context may mask underlying variation in individual behavioral tendencies. Moreover, gene expression patterns may reflect behavioral tendency, while behavioral outcomes are further regulated by social cues perceived in real-time

Advancing Behavioural Genomics by Considering Timescale

Animal behavioural traits often covary with gene expression, pointing towards a genomic constraint on organismal responses to environmental cues. This pattern highlights a gap in our understanding of the time course of environmentally responsive gene expression, and moreover, how these dynamics are regulated. Advances in behavioural genomics explore how gene expression dynamics are correlated with behavioural traits that range from stable to highly labile. We consider the idea that certain genomic regulatory mechanisms may predict the timescale of an environmental effect on behaviour. This temporally minded approach could inform both organismal and evolutionary questions ranging from the remediation of early life social trauma to understanding the evolution of trait plasticity

Insects Provide Unique Systems to Investigate How Early-Life Experience Alters the Brain and Behavior

Early-life experiences have strong and long-lasting consequences for behavior in a surprising diversity of animals. Determining which environmental inputs cause behavioral change, how this information becomes neurobiologically encoded, and the functional consequences of these changes remain fundamental puzzles relevant to diverse fields from evolutionary biology to the health sciences. Here we explore how insects provide unique opportunities for comparative study of developmental behavioral plasticity. Insects have sophisticated behavior and cognitive abilities, and they are frequently studied in their natural environments, which provides an ecological and adaptive perspective that is often more limited in lab-based vertebrate models. A range of cues, from relatively simple cues like temperature to complex social information, influence insect behavior. This variety provides experimentally tractable opportunities to study diverse neural plasticity mechanisms. Insects also have a wide range of neurodevelopmental trajectories while sharing many developmental plasticity mechanisms with vertebrates. In addition, some insects retain only subsets of their juvenile neuronal population in adulthood, narrowing the targets for detailed study of cellular plasticity mechanisms. Insects and vertebrates share many of the same knowledge gaps pertaining to developmental behavioral plasticity. Combined with the extensive study of insect behavior under natural conditions and their experimental tractability, insect systems may be uniquely qualified to address some of the biggest unanswered questions in this field

Mortality risk affects mating decisions in the spider Nephila clavipes

Risk assessment is a fundamental component of any decision-making process, including mate choice. For males, one element of risk that is rarely considered is that a female mate may not survive to offspring independence, resulting in total reproductive failure. This element of risk could be particularly important in short-lived species where all individuals, regardless of condition, attempt to reproduce, and developing mature eggs is a time and energetically expensive process during which females are at risk of predation, starvation, and disease. I evaluate whether males use female survival probability as a mate choice criterion in the golden orb-web spider Nephila clavipes by assessing how male reproductive investment changes depending on female proximity to oviposition. Using a field experiment and a controlled mating experiment, I show that males mate at higher frequencies, transfer more sperm, and father more offspring in the first clutch when mated with nonvirgin females close to oviposition compared with younger nonvirgin females. Furthermore, females close to oviposition have a lower probability of mortality prior to egg deposition compared with virgin females and young nonvirgin adult females. These findings support the hypothesis that males invest more reproductive effort as a female approaches oviposition, possibly because these females are a low-risk mating investment

Altering Social Cue Perception Impacts Honey Bee Aggression With Minimal Impacts on Aggression-Related Brain Gene Expression

Gene expression changes resulting from social interactions may give rise to long term behavioral change, or simply reflect the activity of neural circuitry associated with behavioral expression. In honey bees, social cues broadly modulate aggressive behavior and brain gene expression. Previous studies suggest that expression changes are limited to contexts in which social cues give rise to stable, relatively long-term changes in behavior. Here we use a traditional beekeeping approach that inhibits aggression, smoke exposure, to deprive individuals of aggression-inducing olfactory cues and evaluate whether behavioral changes occur in absence of expression variation in a set of four biomarker genes (drat, cyp6g1/2, GB53860, inos) associated with aggression in previous studies. We also evaluate two markers of a brain hypoxic response (hif1α, hsf) to determine whether smoke induces molecular changes at all. We find that bees with blocked sensory perception as a result of smoke exposure show a strong, temporary inhibition of aggression relative to bees allowed to perceive normal social cues. However, blocking sensory perception had minimal impacts on aggression-relevant gene expression, althought it did induce a hypoxic molecular response in the brain. Results suggest that certain genes differentiate social cue-induced changes in aggression from long-term modulation of this phenotype

A Comparative Analysis of the Morphology and Evolution of Permanent Sperm Depletion in Spiders

Once thought to be energetically cheap and easy to produce, empirical work has shown that sperm is a costly and limited resource for males. In some spider species, there is behavioral evidence that sperm are permanently depleted after a single mating. This extreme degree of mating investment appears to co-occur with other reproductive strategies common to spiders, e.g. genital mutilation and sexual cannibalism. Here we corroborate that sperm depletion in the golden orb-web spider Nephila clavipes is permanent by uncovering its mechanistic basis using light and electron microscopy. In addition, we use a phylogeny-based statistical analysis to test the evolutionary relationships between permanent sperm depletion (PSD) and other reproductive strategies in spiders. Male testes do not produce sperm during adulthood, which is unusual in spiders. Instead, spermatogenesis is nearly synchronous and ends before the maturation molt. Testis size decreases as males approach their maturation molt and reaches its lowest point after sperm is transferred into the male copulatory organs (pedipalps). As a consequence, the amount of sperm available to males for mating is limited to the sperm contained in the pedipalps, and once it is used, males lose their ability to fertilize eggs. Our data suggest that PSD has evolved independently at least three times within web-building spiders and is significantly correlated with the evolution of other mating strategies that limit males to monogamy, including genital mutilation and sexual cannibalism. We conclude that PSD may be an energy-saving adaptation in species where males are limited to monogamy. This could be particularly important in web-building spiders where extreme sexual size dimorphism results in large, sedentary females and small, searching males who rarely feed as adults and are vulnerable to starvation. Future work will explore possible energetic benefits and the evolutionary lability of PSD relative to other mate-limiting reproductive behaviors