Eusociality in snapping shrimps is associated with larger genomes and an accumulation of transposable elements

Abstract

Despite progress uncovering the genomic underpinnings of sociality, much less is known about how social living affects the genome. In different insect lineages, for example, eusocial species show both positive and negative associations between genome size and structure, highlighting the dynamic nature of the genome. Here, we explore the relationship between sociality and genome architecture in Synalpheus snapping shrimps that exhibit multiple origins of eusociality and extreme interspecific variation in genome size. Our goal is to determine whether eusociality leads to an accumulation of repetitive elements and an increase in genome size, presumably due to reduced effective population sizes resulting from a reproductive division of labor, or whether an initial accumulation of repetitive elements leads to larger genomes and independently promotes the evolution of eusociality through adaptive evolution. Using phylogenetically informed analyses, we find that eusocial species have larger genomes with more transposable elements (TEs) and microsatellite repeats than noneusocial species. Interestingly, different TE subclasses contribute to the accumulation in different species. Phylogenetic path analysis testing alternative causal relationships between sociality and genome architecture is most consistent with the hypothesis that TEs modulate the relationship between sociality and genome architecture. Although eusociality appears to influence TE accumulation, ancestral state reconstruction suggests moderate TE abundances in ancestral species could have fueled the initial transitions to eusociality. Ultimately, we highlight a complex and dynamic relationship between genome and social evolution, demonstrating that sociality can influence the evolution of the genome, likely through changes in demography related to patterns of reproductive skew.