Julia B. Saltz

Natural Genetic Variation in Social Niche Construction: Social Effects of Aggression Drive Disruptive Sexual Selection in Drosophila melanogaster

Social niche construction (SNC) occurs when animals actively shape their social environments. Currently the fitness consequences of SNC are poorly understood, and no study has examined whether variation in SNC has a genetic basis. Here we report the first instance of genetic variation in SNC by showing that Drosophila male aggression shapes the social environment. We allowed flies of different genotypes to interact in complex arenas; we measured the number and sex of individuals in the groups that formed and counted instances of mating. Arenas containing more aggressive male genotypes formed groups with fewer males, demonstrating that aggressive male genotypes experienced different social environments than nonaggressive genotypes. Further, genotypes with highest mating success were those whose SNC behavior generated the social environment in which they were most adept at mating: genotypes who mate most often after winning aggressive encounters benefit from aggressive SNC, while genotypes who mate most often after losing achieve high mating rates by forgoing aggression. The presence of these alternative strategies—which were robust across eight population densities—revealed that selection on aggression and context-dependent mating was disruptive, consistent with the hypothesis that SNC can maintain genetic variation in multiple behaviors.

NATURAL GENETIC VARIATION IN SOCIAL ENVIRONMENT CHOICE: CONTEXT‐DEPENDENT GENE–ENVIRONMENT CORRELATION IN DROSOPHILA MELANOGASTER

Gene–environment correlation (rGE) occurs when an individuals genotype determines its choice of environment, generating a correlation between environment and genotype frequency. In particular, social rGE, caused by genetic variation in social environment choice, can critically determine both individual development and the course of social selection. Despite its foundational role in social evolution and developmental psychology theory, natural genetic variation in social environment choice has scarcely been examined empirically. Drosophila melanogaster provides an ideal system for investigating social rGE. Flies live socially in nature and have many opportunities to make social decisions; and natural, heterozygous genotypes may be replicated, enabling comparisons between genotypes across environments. Using this approach, I show that all aspects of social environment choice vary among natural genotypes, demonstrating pervasive social rGE. Surprisingly, genetic variation in group‐size preference was density dependent, indicating that the behavioral and evolutionary consequences of rGE may depend on the context in which social decisions are made. These results provide the first detailed investigation of social rGE, and illustrate that that genetic variation may influence organismal performance by specifying the environment in which traits are expressed.

Natural Variation in Decision-Making Behavior in Drosophila melanogaster

There has been considerable recent interest in using Drosophila melanogaster to investigate the molecular basis of decision-making behavior. Deciding where to place eggs is likely one of the most important decisions for a female fly, as eggs are vulnerable and larvae have limited motility. Here, we show that many natural genotypes of D. melanogaster prefer to lay eggs near nutritious substrate, rather than in nutritious substrate. These preferences are highly polymorphic in both degree and direction, with considerable heritability (0.488) and evolvability. Relative preferences are modulated by the distance between options and the overall concentration of ethanol, suggesting Drosophila integrate many environmental factors when making oviposition decisions. As oviposition-related decisions can be efficiently assessed by simply counting eggs, oviposition behavior is an excellent model for understanding information processing in insects. Associating natural genetic polymorphisms with decision-making variation will shed light on the molecular basis of host choice behavior, the evolutionary maintenance of genetic variation, and the mechanistic nature of preference variation in general.

Three-dimensional tracking and behaviour monitoring of multiple fruit flies

The increasing interest in the investigation of social behaviours of a group of animals has heightened the need for developing tools that provide robust quantitative data. Drosophila melanogaster has emerged as an attractive model for behavioural analysis; however, there are still limited ways to monitor fly behaviour in a quantitative manner. To study social behaviour of a group of flies, acquiring the position of each individual over time is crucial. There are several studies that have tried to solve this problem and make this data acquisition automated. However, none of these studies has addressed the problem of keeping track of flies for a long period of time in three-dimensional space. Recently, we have developed an approach that enables us to detect and keep track of multiple flies in a three-dimensional arena for a long period of time, using multiple synchronized and calibrated cameras. After detecting flies in each view, correspondence between views is established using a novel approach we call the ‘sequential Hungarian algorithm’. Subsequently, the three-dimensional positions of flies in space are reconstructed. We use the Hungarian algorithm and Kalman filter together for data association and tracking. We evaluated rigorously the systems performance for tracking and behaviour detection in multiple experiments, using from one to seven flies. Overall, this system presents a powerful new method for studying complex social interactions in a three-dimensional environment.

Genetic variation in niche construction: implications for development and evolutionary genetics

Niche construction occurs when the traits of an organism influence the environment that it experiences. Research has focused on niche-constructing traits that are fixed within populations or species. However, evidence increasingly demonstrates that niche-constructing traits vary among genotypes within populations. Here, we consider the potential implications of genetic variation in niche construction for evolutionary genetics. Specifically, genetic variation in niche-constructing traits creates a correlation between genotype and environment. Because the environment influences which genes and genetic interactions underlie trait variation, genetic variation in niche construction can alter inferences about the heritability, pleiotropy, and epistasis of traits that are phenotypically plastic. The effects of niche construction on these key evolutionary parameters further suggest novel ways by which niche construction can influence evolution.

Genetic composition of social groups influences male aggressive behaviour and fitness in natural genotypes of Drosophila melanogaster

Indirect genetic effects (IGEs) describe how an individuals behaviour—which is influenced by his or her genotype—can affect the behaviours of interacting individuals. IGE research has focused on dyads. However, insights from social networks research, and other studies of group behaviour, suggest that dyadic interactions are affected by the behaviour of other individuals in the group. To extend IGE inferences to groups of three or more, IGEs must be considered from a group perspective. Here, I introduce the ‘focal interaction’ approach to study IGEs in groups. I illustrate the utility of this approach by studying aggression among natural genotypes of Drosophila melanogaster. I chose two natural genotypes as ‘focal interactants’: the behavioural interaction between them was the ‘focal interaction’. One male from each focal interactant genotype was present in every group, and I varied the genotype of the third male—the ‘treatment male’. Genetic variation in the treatment males aggressive behaviour influenced the focal interaction, demonstrating that IGEs in groups are not a straightforward extension of IGEs measured in dyads. Further, the focal interaction influenced male mating success, illustrating the role of IGEs in behavioural evolution. These results represent the first manipulative evidence for IGEs at the group level.

Genotypic differences in behavioural entropy: unpredictable genotypes are composed of unpredictable individuals

Intra-genotypic variability (IGV) occurs when individuals with the same genotype, raised in the same environment and then tested under the same conditions, express different trait values. Game theoretical and bet-hedging models have suggested two ways that a single genotype might generate variable behaviour when behavioural variation is discrete rather than continuous: behavioural polyphenism (a genotype produces different types of individuals, each of which consistently expresses a different type of behaviour) or stochastic variability (a genotype produces one type of individual who randomly expresses different types of behaviour over time). We first demonstrated significant differences across 14 natural genotypes of male Drosophila melanogaster in the variability (as measured by entropy) of their microhabitat choice, in an experiment in which each fly was allowed free access to four different types of habitat. We then tested four hypotheses about ways that within-individual variability might contribute to differences across genotypes in the variability of microhabitat choice. There was no empirical support for three hypotheses (behavioural polymorphism, consistent choice, or time-based choice), nor could our results be attributed to genotypic differences in activity levels. The stochastic variability hypothesis accurately predicted the slope and the intercept of the relationship across genotypes between entropy at the individual level and entropy at the genotype level. However, our initial version of the stochastic model slightly but significantly overestimated the values of individual entropy for each genotype, pointing to specific assumptions of this model that might need to be adjusted in future studies of the IGV of microhabitat choice. This is among a handful of recent studies to document genotypic differences in behavioural IGV, and the first to explore ways that genotypic differences in within-individual variability might contribute to differences among genotypes in the predictability of their behaviour.

A Bayesian Approach to Social Structure Uncovers Cryptic Regulation of Group Dynamics in Drosophila melanogaster

Understanding the mechanisms that give rise to social structure is central to predicting the evolutionary and ecological outcomes of social interactions. Modeling this process is challenging, because all individuals simultaneously behave in ways that shape their social environments—a process called social niche construction (SNC). In earlier work, we demonstrated that aggression acts as an SNC trait in fruit flies (Drosophila melanogaster), but the mechanisms of that process remained cryptic. Here, we analyze how individual social group preferences generate overall social structure. We use a combination of agent-based simulation and approximate Bayesian computation to fit models to empirical data. We confirm that genetic variation in aggressive behavior influences social group structure. Furthermore, we find that female decamping due to male behavior may play an underappreciated role in structuring social groups. Male-male aggression may sometimes destabilize groups, but it may also be an SNC behavior for shaping desirable groups for females. Density intensifies female social preferences; thus, the role of female behavior in shaping group structure may become more important at high densities. Our ability to model the ontogeny of group structure demonstrates the utility of the Bayesian model–based approach in social behavioral studies.

Nonadditive indirect effects of group genetic diversity on larval viability in Drosophila melanogaster imply key role of maternal decision‐making

Genetic variation can have important consequences for populations: high population genetic diversity is typically associated with ecological success. Some mechanisms that account for these benefits assume that local social groups with high genetic diversity are more successful than low‐diversity groups. At the same time, active decision‐making by individuals can influence group genetic diversity. Here, we examine how maternal decisions that determine group genetic diversity influence the viability of Drosophila melanogaster larvae. Our groups contained wild‐type larvae, whose genetic diversity we manipulated, and genetically marked ‘tester’ larvae, whose genotype and frequency were identical in all trials. We measured wild‐type and tester viability for each group. Surprisingly, the viability of wild‐type larvae was neither augmented nor reduced when group genetic diversity was altered. However, the viability of the tester genotype was substantially depressed in large, high‐diversity groups. Further, not all high‐diversity groups produced this effect: certain combinations of wild‐type genotypes were deleterious to tester viability, while other groups of the same diversity—but containing different wild‐type genotypes—were not deleterious. These deleterious combinations of wild‐type genotypes could not be predicted by observing the performance of the same tester and wild‐type genotypes in low‐diversity groups. Taken together, these results suggest that nonadditive interactions among genotypes, rather than genetic diversity per se, account for between‐group differences in viability in D. melanogaster and that predicting the consequences of genetic diversity at the population level may not be straightforward.

Genetic Correlations among Developmental and Contextual Behavioral Plasticity in Drosophila melanogaster

Correlations among traits, including behaviors, are important because traits that are genetically correlated may not evolve independently. Recently, behavioral-correlations research has expanded to include correlations not only in mean-level behaviors but also in behavioral plasticity, that is, the degree to which individuals change their behavior in response to environmental stimuli. Positive correlations among behavioral plasticities would imply that individuals or genotypes that are behaviorally plastic in one way may also be plastic in other ways; negative correlations could imply trade-offs. Here, we examine aversive odor conditioning (learning) at two time points and plasticity in pupation site selection behavior across substrates in a panel of Drosophila genotypes. These behaviors represent different types of behavioral plasticity: contextual plasticity describes behavioral responses to stimuli that are currently present, while developmental plasticity describes behavioral responses to remembered experiences with stimuli in the recent past. We find that learning scores and plasticity in pupation site selection behavior are positively genetically correlated, representing the first example of a genetic correlation between developmental and contextual plasticity. These findings imply that ecological and evolutionary theories focusing on variation in a single dimension of behavioral plasticity may be incomplete.