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

Abstract

Are eusociality and extraordinary aging polyphenisms evolutionarily coupled? The remarkable disparity in longevity between social insect queens and sterile workers—decades vs. months, respectively—has long been recognized. In mammals, the lifespan of eusocial naked mole rats is extremely long—roughly 10 times greater than that of mice. Is this robustness to senescence associated with social evolution and shared mechanisms of developmental timing, neuroprotection, antioxidant defenses, and neurophysiology? Focusing on brain senescence, we examine correlates and consequences of aging across two divergent eusocial clades and how they differ from solitary taxa. Chronological age and physiological indicators of neural deterioration, including DNA damage or cell death, appear to be decoupled in eusocial insects. In some species, brain cell death does not increase with worker age and DNA damage occurs at similar rates between queens and workers. In comparison, naked mole rats exhibit characteristics of neonatal mice such as protracted development that may offer protection from aging and environmental stressors. Antioxidant defenses appear to be regulated differently across taxa, suggesting independent adaptations to life history and environment. Eusocial insects and naked mole rats appear to have evolved different mechanisms that lead to similar senescence-resistant phenotypes. Careful selection of comparison taxa and further exploration of the role of metabolism in aging can reveal mechanisms that preserve brain functionality and physiological resilience in eusocial species.

Social Brain Energetics: Ergonomic Efficiency, Neurometabolic Scaling, and Metabolic Polyphenism in Ants

“…Queens, for example, may be several orders of magnitude larger than workers. Queens, workers, and males also vary significantly in longevity ( Kramer and Schaible 2013 ) and worker longevity is associated with reduced mass-specific worker metabolic rates ( Giraldo et al 2021 ). Metabolic tradeoffs may be minimized by distributing reproductive and non-reproductive physiologies in different-size bodies ( Friedman et al 2020 ).…”

“…If worker production costs are relatively higher than worker maintenance costs, selection may favor increased worker longevity. However, increased risk of mortality may select for reduced longevity ( Giraldo et al 2021 ). The evolution of major workers as defensive specialists may reduce the risk of extrinsic mortality and relax such selection.…”

Editorial: Mechanisms and Pathways Contributing to the Diversity of Aging Across the Tree of Life

“…Increased sociality is associated with a longer lifespan ( see ( Arnold and Owens 1998 ; Thorley 2020 ) for examples) and eusociality, in particular, presents a fascinating window into the evolution of aging with greatly extended lifespans compared to non-social relatives, but also diversity in aging among castes ( Keller and Jemielity 2006 ; Kramer et al, 2016 ). Giraldo and others ( Giraldo et al, 2021 ) provide a mini-review examining the relationship between eusociality and brain senescence in eusocial species. They conclude that, though different taxa may show similarly extended lifespans and similar senescence phenotypes, the mechanisms involved are different.…”

Mechanisms and Pathways Contributing to the Diversity of Aging across the Tree of Life

“…Increased sociality is associated with a longer lifespan (see (Arnold and Owens 1998;Thorley 2020) for examples) and eusociality, in particular, presents a fascinating window into the evolution of aging with greatly extended lifespans compared to non-social relatives, but also diversity in aging among castes (Keller and Jemielity 2006;Kramer et al, 2016). Giraldo and others (Giraldo et al, 2021) provide a minireview examining the relationship between eusociality and brain senescence in eusocial species. They conclude that, though different taxa may show similarly extended lifespans and similar senescence phenotypes, the mechanisms involved are different.…”