Social reprogramming in ants induces longevity-associated glia remodeling

Abstract

In social insects, workers and queens arise from the same genome but display profound differences in behavior and longevity. In Harpegnathos saltator ants, adult workers can transition to a queen-like state called gamergate, which results in reprogramming of social behavior and life-span extension. Using single-cell RNA sequencing, we compared the distribution of neuronal and glial populations before and after the social transition. We found that the conversion of workers into gamergates resulted in the expansion of neuroprotective ensheathing glia. Brain injury assays revealed that activation of the damage response gene Mmp1 was weaker in old workers, where the relative frequency of ensheathing glia also declined. On the other hand, long-lived gamergates retained a larger fraction of ensheathing glia and the ability to mount a strong Mmp1 response to brain injury into old age. We also observed molecular and cellular changes suggestive of age-associated decline in ensheathing glia in Drosophila.

(Epi)Genetic Mechanisms Underlying the Evolutionary Success of Eusocial Insects

“…Non-reproductive females possess larger brains and inactivated ovaries, while reproductive females generally experience a reduced brain size, but much larger activated ovaries. Representative genes from all major eusocial insect lineages are listed here, including genes from ants [31][32][33][34]37,73,74], bees [75][76][77][78][79][80], social wasps [81,82], and termites [72].…”

“…Non-reproductive H. saltator ant workers may undergo transition into fertile pseudoqueens ("gamergates") (Table 1) without experiencing genomic change. The transition is accompanied by a change in nervous cell composition, e.g., with gamergates experiencing a~40% increase in neuroprotective ensheathing glial cells in the brain [73]. This change in cellular composition may contribute to an increased longevity in gamergates, fivefold in comparison to workers, by allowing the brain to actively respond to damage as the individual ages [73].…”

“…The transition is accompanied by a change in nervous cell composition, e.g., with gamergates experiencing a~40% increase in neuroprotective ensheathing glial cells in the brain [73]. This change in cellular composition may contribute to an increased longevity in gamergates, fivefold in comparison to workers, by allowing the brain to actively respond to damage as the individual ages [73]. In addition, a damage responsive gene Mmp-1 is upregulated in gamergates, providing a molecular mechanism responsible for their longer lifespan [73].…”

“…This change in cellular composition may contribute to an increased longevity in gamergates, fivefold in comparison to workers, by allowing the brain to actively respond to damage as the individual ages [73]. In addition, a damage responsive gene Mmp-1 is upregulated in gamergates, providing a molecular mechanism responsible for their longer lifespan [73]. Gene expression changes in the ovaries and fat bodies occur, preluded by initial gene expression changes in the brain of the transitioning individual.…”

Eusociality and Senescence: Neuroprotection and Physiological Resilience to Aging in Insect and Mammalian Systems

“…Glia may offer neuroprotection. Aging D. melanogaster and H. saltator workers show decreases in gene expression for transcripts that characterize ensheathing glia ( Sheng et al, 2020 ), which in Drosophila respond to injury ( Doherty et al, 2009 ; Kato et al, 2011 , 2018 ) and decline in function with increasing age ( Purice et al, 2016 ). However, age-matched H. saltator reproductives exhibit a higher proportion of these glia, suggesting a neuroprotective role.…”