Evolution of ageing, costs of reproduction and the fecundity–longevity trade-off in eusocial insects

Abstract

Eusocial insects provide special opportunities to elucidate the evolution of ageing as queens have apparently evaded costs of reproduction and reversed the fecundity–longevity trade-off generally observed in non-social organisms. But how reproduction affects longevity in eusocial insects has rarely been tested experimentally. In this study, we took advantage of the reproductive plasticity of workers to test the causal role of reproduction in determining longevity in eusocial insects. Using the eusocial bumblebee Bombus terrestris, we found that, in whole colonies, in which workers could freely ‘choose’ whether to become reproductive, workers' level of ovarian activation was significantly positively associated with longevity and ovary-active workers significantly outlived ovary-inactive workers. By contrast, when reproductivity was experimentally induced in randomly selected workers, thereby decoupling it from other traits, workers' level of ovarian activation was significantly negatively associated with longevity and ovary-active workers were significantly less long-lived than ovary-inactive workers. These findings show that workers experience costs of reproduction and suggest that intrinsically high-quality individuals can overcome these costs. They also raise the possibility that eusocial insect queens exhibit condition-dependent longevity and hence call into question whether eusociality entails a truly reversed fecundity–longevity trade-off involving a fundamental remodelling of conserved genetic and endocrine networks underpinning ageing.

Transcriptional profile and differential fitness in a specialist milkweed insect across host plants varying in toxicity

“…Comparing milkweed species that vary more substantially in cardenolide toxicity, we found that host plants with increased and more nonpolar cardenolides have negative effects on A. nerii development and fecundity, consistent with other studies that have demonstrated that plant species characterized by more toxic cardenolides are negatively associated with A. nerii population growth (Agrawal, ; Colvin, Snyder, & Thacker, ; de Roode et al., ). In the first fitness experiment, there was evidence of greater longevity on more highly defended plants (Figure e), perhaps indicative of trade‐offs between fecundity and longevity (Blacher, Huggins, & Bourke, ; Miyatake, ). However, we interpret this result with caution, both because the effect was not replicated in the second experiment (Fig.…”

The scaling of expansive energy under the Red Queen predicts Cope’s Rule

“…While specialized life history strategies are widely recognized (Sibly and Brown 2009), birth rates are governed by metabolic scaling (Lindstedt and Calder 1981) and are not easy to change permanently without physiological tradeoffs. Elevated reproductive rates lead to shortened lifespan, as limited resources enforce a compromise between investment in reproduction and somatic maintenance (Edward and Chapman 2011, Blacher et al 2017).…”

Role of Hormones in the Control of Reproductive Physiology and Reproductive Behavior

“…Reproduction itself is central to the Evolution of species [1]. Indeed, it is the slow drift of genotypes along successive generations of living species that gives rise to increasing variability of individuals, and occasio to speciation [2][3][4][5][6]. Speciation occurs when individuals from the same original species become unable to interbreed (and thus do not reproduce).…”