Developmental plasticity shapes social traits and selection in a facultatively eusocial bee

Developmental plasticity generates phenotypic variation, but how it contributes to evolutionary change is unclear. Phenotypes of individuals in caste-based (eusocial) societies are particularly sensitive to developmental processes, and the evolutionary origins of eusociality may be rooted in developmental plasticity of ancestral forms. We used an integrative genomics approach to evaluate the relationships among developmental plasticity, molecular evolution, and social behavior in a bee species (Megalopta genalis) that expresses flexible sociality, and thus provides a window into the factors that may have been important at the evolutionary origins of eusociality. We find that differences in social behavior are derived from genes that also regulate sex differentiation and metamorphosis. Positive selection on social traits is influenced by the function of these genes in development. We further identify evidence that social polyphenisms may become encoded in the genome via genetic changes in regulatory regions, specifically in transcription factor binding sites. Taken together, our results provide evidence that developmental plasticity provides the substrate for evolutionary novelty and shapes the selective landscape for molecular evolution in a major evolutionary innovation: Eusociality

Cumulative Effects of Spontaneous Mutations for Fitness in Caenorhabditis: Role of Genotype, Environment and Stress

It is often assumed that the mutation rate is an evolutionarily optimized property of a taxon. The relevant mutation rate is for mutations that affect fitness, U, but the strength of selection on the mutation rate depends on the average effect of a mutation. Determination of U is complicated by the possibility that mutational effects depend on the particular environmental context in which the organism exists. It has been suggested that the effects of deleterious mutations are typically magnified in stressful environments, but most studies confound genotype with environment, so it is unclear to what extent environmental specificity of mutations is specific to a particular starting genotype. We report a study designed to separate effects of species, genotype, and environment on the degradation of fitness resulting from new mutations. Mutations accumulated for >200 generations at 20° in two strains of two species of nematodes that differ in thermal sensitivity. Caenorhabditis briggsae and C. elegans have similar demography at 20°, but C. elegans suffers markedly reduced fitness at 25°. We find little evidence that mutational properties differ depending on environmental conditions and mutational correlations between environments are close to those expected if effects were identical in both environments

Mutational Bias for Body Size in Rhabditid Nematodes

Mutational bias is a potentially important agent of evolution, but it is difficult to disentangle the effects of mutation from those of natural selection. Mutation-accumulation experiments, in which mutations are allowed to accumulate at very small population size, thus minimizing the efficiency of natural selection, are the best way to separate the effects of mutation from those of selection. Body size varies greatly among species of nematode in the family rhabditidae; mutational biases are both a potential cause and a consequence of that variation. We report data on the cumulative effects of mutations that affect body size in three species of rhabditid nematode that vary fivefold in adult size. Results are very consistent with previous studies of mutations underlying fitness in the same strains: two strains of Caenorhabditis briggsae decline in body size about twice as fast as two strains of C. elegans, with a concomitant higher point estimate of the genomic mutation rate; the confamilial Oscheius myriophila is intermediate. There is an overall mutational bias, such that mutations reduce size on average, but the bias appears consistent between species. The genetic correlation between mutations that affect size and those underlying fitness is large and positive, on average

Genomic regions influencing aggressive behavior in honey bees are defined by colony allele frequencies

For social animals, the genotypes of group members affect the social environment, and thus individual behavior, often indirectly. We used genome-wide association studies (GWAS) to determine the influence of individual vs. group genotypes on aggression in honey bees. Aggression in honey bees arises from the coordinated actions of colony members, primarily nonreproductive "soldier" bees, and thus, experiences evolutionary selection at the colony level. Here, we show that individual behavior is influenced by colony environment, which in turn, is shaped by allele frequency within colonies. Using a population with a range of aggression, we sequenced individual whole genomes and looked for genotype–behavior associations within colonies in a common environment. There were no significant correlations between individual aggression and specific alleles. By contrast, we found strong correlations between colony aggression and the frequencies of specific alleles within colonies, despite a small number of colonies. Associations at the colony level were highly significant and were very similar among both soldiers and foragers, but they covaried with one another. One strongly significant association peak, containing an ortholog of the Drosophila sensory gene dpr4 on linkage group (chromosome) 7, showed strong signals of both selection and admixture during the evolution of gentleness in a honey bee population. We thus found links between colony genetics and group behavior and also, molecular evidence for group-level selection, acting at the colony level. We conclude that group genetics dominates individual genetics in determining the fatal decision of honey bees to sting.Funding provided by: Office of Extramural Research, National Institutes of HealthCrossref Funder Registry ID: http://dx.doi.org/10.13039/100006955Award Number: R01GM11746