Are personalities genetically determined? Inferences from subsocial spiders.

BACKGROUND:Recent research has revealed that polymorphic behavioral strategies shape intra-and interspecific interactions and contribute to fitness in many animal species. A better understanding of the proximate mechanisms underlying these behavioral syndromes will enhance our grasp this phenomenon. Spiders in the genus Anelosimus exhibit inter-individual behavioral variation on several axes: individuals have consistent responses to stimuli (e.g. bold vs. shy individuals) and they are subsocial (exhibiting extended maternal care and sibling cooperation) across most of their range, but they sometimes form permanent social groups in northern temperate regions. Here, we seek genetic variants associated with boldness and with social structure in a socially polymorphic population of the spider Anelosimus studiosus. We also develop preliminary genomic resources, including a genome assembly and linkage map, that support this and future genomic research on this group. RESULTS:Remarkably, we identify a small genomic scaffold (~ 1200 bp) that harbors seven single nucleotide polymorphisms (SNPs) associated with boldness. Moreover, heterozygotes are less common than expected based on Hardy-Weinberg equilibrium, suggesting that either assortative mating or selection against heterozygotes may be occurring in this system. We find no loci significantly associated with social organization. Our draft genome assembly allows us to localize SNPs of interest in this study and to carry out genetic comparisons with other published genomes, although it remains highly fragmented. CONCLUSIONS:By identifying a locus associated with a well-studied animal personality trait, this study opens up avenues for future research to link behavioral studies of animal personality with genotype and fitness

Insights from the study of complex systems for the ecology and evolution of animal populations

D.N.F. thanks Jack W. Bradbury and Sandra L. Vehrencamp for writing the article that originally stimulated his thoughts in this area. The authors are also grateful to Simon Denomme-Brown, Gustavo Betini and Elizabeth Hobson for reviewing drafts of this article, and Andrew G. McAdam for allowing D.N.F. to pursue this project despite employing him to study squirrels. Four anonymous reviewers provided useful comments that helped improve the manuscript. We have no conflicting interests.Peer reviewedPublisher PD

Evidence of social niche construction: persistent and repeated social interactions generate stronger personalities in a social spider.

While there are now a number of theoretical models predicting how consistent individual differences in behaviour may be generated and maintained, so far, there are few empirical tests. The social niche specialization hypothesis predicts that repeated social interactions among individuals may generate among-individual differences and reinforce within-individual consistency through positive feedback mechanisms. Here, we test this hypothesis using groups of the social spider Stegodyphus mimosarum that differ in their level of familiarity. In support of the social niche specialization hypothesis, individuals in groups of spiders that were more familiar with each other showed greater repeatable among-individual variation in behaviour. Additionally, individuals that were more familiar with each other exhibited lower within-individual variation in behaviour, providing one of the first examples of how the social environment can influence behavioural consistency. Our study demonstrates the potential for the social environment to generate and reinforce consistent individual differences in behaviour and provides a potentially general mechanism to explain this type of behavioural variation in animals with stable social groups

Individual and Group Performance Suffers from Social Niche Disruption.

The social niche specialization hypothesis predicts that animal personalities emerge as a result of individuals occupying different social niches within a group. Here we track individual personality and performance and collective performance among groups of social spiders where we manipulated the familiarity of the group members. We show that individual personalities, as measured by consistent individual differences in boldness behavior, strengthen with increasing familiarity and that these personalities can be disrupted by a change in group membership. Changing group membership negatively impacted both individual and group performance. Individuals in less familiar groups lost weight, and these groups were less successful at performing vital collective tasks. These results provide a mechanism for the evolution of stable social groups by demonstrating that social niche reestablishment carries a steep cost for both individuals and groups. Social niche specialization may therefore provide a potential first step on the path toward more organized social systems

Genetic Changes to a Transcriptional Silencer Element Confers Phenotypic Diversity within and between Drosophila Species

The modification of transcriptional regulation has become increasingly appreciated as a major contributor to morphological evolution. However, the role of negative-acting control elements (e.g. silencers) in generating morphological diversity has been generally overlooked relative to positive-acting “enhancer” elements. The highly variable body coloration patterns among Drosophilid insects represents a powerful model system in which the molecular alterations that underlie phenotypic diversity can be defined. In a survey of pigment phenotypes among geographically disparate Japanese populations of Drosophila auraria, we discovered a remarkable degree of variation in male-specific abdominal coloration. In testing the expression patterns of the major pigment-producing enzymes, we found that phenotypes uniquely correlated with differences in the expression of ebony, a gene required for yellow-colored cuticle. Assays of ebony’s transcriptional control region indicated that a lightly pigmented strain harbored cis-regulatory mutations that caused correlated changes in its expression. Through a series of chimeric reporter constructs between light and dark strain alleles, we localized function-altering mutations to a conserved silencer that mediates a male-specific pattern of ebony repression. This suggests that the light allele was derived through the loss of this silencer’s activity. Furthermore, examination of the ebony gene of D. serrata, a close relative of D. auraria which secondarily lost male-specific pigmentation revealed the parallel loss of this silencer element. These results demonstrate how loss-of-function mutations in a silencer element resulted in increased gene expression. We propose that the mutational inactivation of silencer elements may represent a favored path to evolve gene expression, impacting morphological traits

Collective aggressiveness limits colony persistence in high‐ but not low‐elevation sites at Amazonian social spiders

Identifying the traits that foster group survival in contrasting environments is important for understanding local adaptation in social systems. Here, we evaluate the relationship between the aggressiveness of social spider colonies and their persistence along an elevation gradient using the Amazonian spider, Anelosimus eximius. We found that colonies of A. eximius exhibit repeatable differences in their collective aggressiveness (latency to attack prey stimuli) and that colony aggressiveness is linked with persistence in a site‐specific manner. Less aggressive colonies are better able to persist at high‐elevation sites, which lack colony‐sustaining large‐bodied prey, whereas colony aggression was not related to chance of persistence at low‐elevation sites. This suggests that low aggressiveness promotes colony survival in high‐elevation, prey‐poor habitats, perhaps via increased tolerance to resource limitation. These data reveal that the collective phenotypes that relate to colony persistence vary by site, and thus, the path of social evolution in these environments is likely to be affected.Colony‐level selection on collective aggressiveness varies with elevation in social spiders. Aggressive societies are disfavoured at high elevation sites, but their odds of persistence increase in lowland rain forests.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/152489/1/jeb13532_am.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/152489/2/jeb13532.pd

Within-group behavioral variation promotes biased task performance and the emergence of a defensive caste in a social spider

The social spider Anelosimus studiosus exhibits a behavioral polymorphism where colony members express either a passive, tolerant behavioral tendency (social) or an aggressive, intolerant behavioral tendency (asocial). Here we test whether asocial individuals act as colony defenders by deflecting the suite of foreign (i.e., heterospecific) spider species that commonly exploit multi-female colonies. We (1) determined whether the phenotypic composition of colonies is associated with foreign spider abundance, (2) tested whether heterospecific spider abundance and diversity affect colony survival in the field, and (3) performed staged encounters between groups of A. studiosus and their colony-level predator Agelenopsis emertoni (A. emertoni)to determine whether asocial females exhibit more defensive behavior. We found that larger colonies harbor more foreign spiders, and the number of asocial colony members was negatively associated with foreign spider abundance. Additionally, colony persistence was negatively associated with the abundance and diversity of foreign spiders within colonies. In encounters with a colony-level predator, asocial females were more likely to exhibit escalatory behavior, and this might explain the negative association between the frequency of asocial females and the presence of foreign spider associates. Together, our results indicate that foreign spiders are detrimental to colony survival, and that asocial females play a defensive role in multi-female colonies

Social interactions shape individual and collective personality in social spiders

The behavioural composition of a group and the dynamics of social interactions can both influence how social animals work collectively. For example, individuals exhibiting certain behavioural tendencies may have a disproportionately large impact on the group, and so are referred to as keystone individuals, while interactions between individuals can facilitate information transmission about resources. Despite the potential impact of both behavioural composition and interactions on collective behaviour, the relationship between consistent behaviours, also known as personalities, and social interactions remains poorly understood. Here, we use stochastic actor oriented models to uncover the interdependencies between boldness and social interactions in the social spider Stegodyphus dumicola. We find that boldness has no effect on the likelihood of forming social interactions, but interactions do affect boldness, and lead to an increase in the boldness of the shyer individual. Furthermore, spiders tend to interact with the same individuals as their neighbours. In general, boldness decreases over time but once an individual's boldness begins to increase, this increase accelerates, suggesting a positive feedback mechanism. These dynamics of interactions and boldness result in skewed boldness distributions of a few bold individuals and many shy individuals, as observed in nature. This group behavioural composition facilitates efficient collective behaviours, such as rapid collective prey attack. Thus, by examining the relationship between behaviour and interactions, we reveal the mechanisms that underlie the emergence of adaptive group composition and collective behaviour