Karen M. Kapheim,  Beryl M. Jones,  Hailin Pan, Cai Li,  Brock A. Harpur,  Clement F. Kent,  Amro Zayed,  Panagiotis Ioannidis, Robert M. Waterhouse, Callum Kingwell,  Eckart Stolle,  Arián Avalos, Guojie Zhang, W. Owen McMillan, and William T. Wcislo

PNAS June 16, 2020 117 (24) 13615-13625 - ECOLOGY

Significance

Developmental processes are an important source of phenotypic variation, but the extent to which this variation contributes to evolutionary change is unknown. We used integrative genomic analyses to explore the relationship between developmental and social plasticity in a bee species that can adopt either a social or solitary lifestyle. We find genes regulating this social flexibility also regulate development, and positive selection on these genes is influenced by their function during development. This suggests that developmental plasticity may influence the evolution of sociality. Our additional finding of genetic variants linked to differences in social behavior sheds light on how phenotypic variation derived from development may become encoded into the genome, and thus contribute to evolutionary change.

Abstract

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.

See https://www.pnas.org/content/117/24/13615

Figure 2: Correlation of logFC across life stages, sexes, and social phenotypes. Differential expression of genes from each pair of conditions was compared to all other pairs to identify contrasts with significantly similar gene-expression changes. Circle size and color represent correlation strength (Spearman’s ρ); positive or negative correlation indicates concordance or discordance in direction of differential expression, depending on order in which the dyad is listed (e.g., QvW vs. WvR in red indicates a similar set of genes is up-regulated in Q and R compared with W); boxes highlight expression changes during development correlated with expression differences in abdominal (orange) or brain (green) tissue among social types; empty cells indicate correlations were not statistically significant (Benjamini–Hochberg adjusted P < 0.001); correlation and P values are in Dataset S5.