Abstract: A group's composition is important for its success. Colonies of the spider Anelosimus studiosus appear to have responded to this pressure by evolving the ability to maintain mixtures of docile versus aggressive individuals that help colonies avoid extinction. Here we demonstrate that colony extinction events unite the optimal group composition of all colony constituents, regardless of phenotype, with that of the colony as a whole. This is because colony extinction events explain the majority of individual mortality events in A. studiosus. Through within- and across-habitat colony manipulations, we further determined that reduction in reproductive output by individuals bearing overabundant phenotypes underlies the ability of colonies to adaptively regulate their compositions. When we experimentally created colonies with an overabundance of the docile or aggressive phenotype, individuals bearing the overabundant phenotype exhibited reduced reproductive output, which helped to move colony compositions back towards their site-specific optima. Colonies displaced from their native sites continued to recreate the patterns of reproductive output that characterized their site of origin, suggesting a genetic component to this trait. Individuals thus appear to adaptively cull their reproductive output depending on their phenotype and the composition of their colony. There is also considerable parent–offspring colony resemblance in the extent to which colonies can or do track their ideal compositions. This conveys a kind of collective heritability to this trait. Together, while group selection appears to be the principal driver of ongoing selection on group composition in A. studiosus, patterns of selection among individuals within groups appear to promote colonies' ability to track their ideal mixtures.
Abstract: In Pruitt and Goodnight1 we provided experimental evidence that group selection has contributed to a group-level adaptation in the social spider Anelosimus studiosus. Grinsted et al.2 provide a wide diversity of system-specific critiques of our original study. In contrast, Gardner3 highlights differences between our definition of ‘group level adaptations’ and his own. He further describes a model that recreates some of the dynamics seen in Anelosimus studiosus. Below, we address the critiques of Grinsted et al.2 first and Gardner3 second.
Abstract: Group selection may be defined as selection caused by the differential extinction or proliferation of groups1,2. The socially polymorphic spider Anelosimus studiosus exhibits a behavioural polymorphism in which females exhibit either a ‘docile’ or ‘aggressive’ behavioural phenotype3,4. Natural colonies are composed of a mixture of related docile and aggressive individuals, and populations differ in colonies’ characteristic docile:aggressive ratios5,6. Using experimentally constructed colonies of known composition, here we demonstrate that population-level divergence in docile:aggressive ratios is driven by site-specific selection at the group level—certain ratios yield high survivorship at some sites but not others. Our data also indicate that colonies responded to the risk of extinction: perturbed colonies tended to adjust their composition over two generations to match the ratio characteristic of their native site, thus promoting their long-term survival in their natal habitat. However, colonies of displaced individuals continued to shift their compositions towards mixtures that would have promoted their survival had they remained at their home sites, regardless of their contemporary environment. Thus, the regulatory mechanisms that colonies use to adjust their composition appear to be locally adapted. Our data provide experimental evidence of group selection driving collective traits in wild populations.