Nutritional specialization and social evolution in woodroaches and termites.

Woodroach biparental care and termite sibling altruism evolved from solitary cockroach ancestors after nutritional specialization on nutrient-deficient deadwood, but the accompanying genomic changes remained unclear. We sequenced eight new species of the order Blattodea, showing stepwise contracted genomes. Woodroach brood rearing remained constrained by deactivated oxidative phosphorylation and peroxisome genes, consistent with slow immature growth. Termites lost key genes that mediate sperm motility, corroborating that reproductive division of labor required monogamous colony founding. They also co-opted many genes from fundamental nutrition-sensitive juvenile hormone, insulin, epidermal growth factor receptor (EGFR), and Decapentaplegic (Dpp) signaling pathways. Thus, most larvae develop as workers by means of high energy metabolism early on, whereas reproductive nymphs highly express energy metabolism genes late in development. These pathways are consistent with obligate dependence on provisioning by specialized workers and feedback loops that allow large homeostatic colonies to evolve. Editor's summary: The evolution of reproductive division of labor such as in social insects like bees has occurred multiple times, although the genomic mechanisms supporting these transitions remain unclear. Cui et al. sequenced the genomes of three cockroach and five termite species and compared them with seven previously generated genomes. The authors found that termites had smaller genomes with fewer genes than roaches, including genes related to sperm motility and diet specialization. They also collected gene expression and developmental data for several previously uncharacterized species, which will serve as a resource for future studies. —Corinne Simonti INTRODUCTION: Social evolution theory makes numerous testable predictions for the expression of reproductive altruism for indirect fitness benefits. Studies of ants, bees, and wasps have amply corroborated the validity of the theory, but termites have been neglected, despite outbred monogamous colony founding and full-sibling relatedness being the norm. RATIONALE: Our integrated genomic and transcriptomic study clarifies the evolution of biparental care, conditional altruism, and obligate altruism across the order Blattodea. We obtained 15 cockroach, woodroach, and termite genomes and transcriptomes to assess the gene gains or losses associated with changes in diet and habitat, and to map metabolic efficiency across developmental stages. We focused on functional analyses in three species representing distinct stages of (pre)social evolution: an omnivorous solitary Periplaneta cockroach, a wood-dwelling Cryptocercus woodroach with biparental care, and a foraging Reticulitermes termite with bifurcated caste differentiation. RESULTS: We document substantial gene family contractions and gene losses, often associated with nutrition and metabolism, both at the origin of wood-feeding and biparental care and at the emergence of termite sibling altruism. Many cilium- and flagellum-associated genes were lost throughout termites, consistent with the loss of monoflagellar spermatozoa after monogamous colony founding and with the emergence of sibling altruism in termites but not in sexually promiscuous Cryptocercus. Using transcriptomes, we further show that slow-growing woodroaches have constrained energy metabolism because oxidative phosphorylation and peroxisome genes are deactivated. By contrast, energy metabolism in Reticulitermes termites is more efficient and has evolved to be variable between castes. Energy metabolism and juvenile hormone (JH) signaling are high during early worker development, whereas high energy metabolism combines with low JH signaling during late reproductive development. Reticulitermes termites achieved these caste-differentiated adjustments through co-option of fundamental nutrition-sensitive insulin, epidermal growth factor receptor (EGFR), and target of rapamycin complex 1 (TORC1) pathways, resembling cockroach rather than woodroach ancestry. Controlled breeding showed that time-differentiated provisioning of larvae with different caste potential induces feedback loops to prioritize mass production of workers, whereas rearing reproductives remains a secondary priority. Transcriptomics of linearly developing larvae in the wood-dwelling nonforaging termite Cryptotermes declivis, where sibling altruism remained condition dependent, showed that metabolic activity is intermediate between that of Cryptocercus and Reticulitermes. CONCLUSION: Our results match the prediction that monogamy was a necessary condition for the evolution of conditional altruism in wood-dwelling termites. However, colony-founding monogamy was not sufficient for the evolution of unconditional altruism by a specialized worker caste unless full-sibling family structure continued throughout the colony life cycle. That threshold was likely passed when termites such as Reticulitermes evolved territorial foraging, which likely precluded secondary colony mergers so that bifurcated caste differentiation and worker sterility could evolve, controlled by metabolically enhanced and differentially JH-regulated nutritional provisioning. Evolution of woodroach biparental care and termite sibling altruism.: After the evolution of nutritional specialization on deadwood, metabolism-related gene families contracted in woodroaches and termites. Promisicuous woodroaches evolved biparental care under constrained energy metabolism, whereas monogamous termites evolved a sterile worker caste after losing many cilium- and flagellum-associated genes, rendering sperm immotile. Co-option of ancestral nutrition-sensitive JH-signaling and energy-metabolism genes ultimately led to ergonomically efficient bifurcated caste differentiation. [ABSTRACT FROM AUTHOR]