Are personalities genetically determined? Inferences from subsocial spiders

Abstract

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.

Keywords: Animal personality; Boldness; Genome assembly; Linkage map; RADseq; Social spiders.

Fig. 1

Principal component analyses of genetic structure between mother and offspring from family P1 (a) and family P2 (b) reveal a pattern consistent with multiple paternity of offspring. In both cases, the mother (enlarged black dot) is positioned between two offspring clusters (open dots) that are separated along principal component axis 1. For a follow-up assessment of relatedness (Additional file 1: Figure S2), we consider individuals with PC axis 1 values less than the mother to be putative full sib group 1, and those with values greater than the mother to be full sib group 2

Fig. 2

Comparison of boldness score by genotype (a) in individuals at the most highly associated locus of seven highly significant SNPs on scaffold 422,272 (enlarged red dot, B). The outlier loci on the boxplots are shown with light grey open circles, while all data points (including outliers) are shown as jittered, black filled circles. The QQ plot (b) compares the expected and observed p-values with the grey bar indicating 95% confidence intervals, revealing that the observed associations exhibit more significant p-values than expected by chance

Fig. 3

The four sampling localities in eastern Tennessee are shown with orange stars (a), and the total number of nests collected that were either solitary (blue) or social (green) are shown with pie charts. The distribution of latency to move after perturbation (a measure of boldness) is shown for individuals from each of the four populations (b: Melton Lake, c: Melton Hill, d: Boone Lake, and e: Chilhowee Dam). Individuals that moved quickly (low latency score) are bold, whereas individuals with a slow response (high latency score) are shy. There was no association between nest type (social or solitary) and boldness; populations differed in the frequency of the alternate allele at the locus that is most strongly associated with boldness