“Plastic senescence in the honeybee and the disposable soma theory”

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Jack da Silva (Sep 2019)

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The lifespan differences between honeybee castes help distinguish between different evolutionary theories of ageing

Honeybee workers ageing faster than the queen points to a specific evolutionary theory of ageing

A honeybee (Apis mellifera) worker performing the high-risk duties of a forager.
(Credit: Paul van de Velde. Reproduced under the Creative Commons BY 2.0 License. https://www.flickr.com/photos/dordrecht-holland/20547107253)

Honeybee workers have much shorter lifespans than the queen not simply because they live more dangerous lives, but because they age faster. This tells us that ageing evolves as a consequence of an organism’s life history being adapted to its environment.

Designation of an individual as a worker or a queen is not based on different sets of genes but on nutrition – a larva that is fed a protein-rich diet develops into a queen, otherwise she develops into a worker. As a worker, a bee ages so rapidly that she typically lives for only one month. In contrast, a queen may live for two years. But why should workers age more rapidly? Evolutionary theories of ageing tell us that natural selection becomes weaker with age simply because any individual has a lower probability of surviving to an old age than to a young age for reasons unrelated to ageing, such as accidental death. As a result, natural selection is less efficient at removing mutations that reduce survival or fertility at older ages, which may explain ageing. It follows from this that species that live more dangerous lives should age more rapidly. This logic also applies to honeybee workers, who perform high-risk duties outside the hive. However, since the designation of a worker is not based on a genetic difference from the queen, its higher rate of ageing must be due to different genes being turned on. The genes that are turned on in a worker are thought to invest the energy in its food in maintaining the bee’s body just enough to keep it functioning for its expected short lifespan, and as a result the bee ages rapidly. Any greater investment in maintenance would be wasteful. These results support an evolutionary theory of ageing, known as the disposable soma theory, that explains ageing as the consequence of organisms evolving an optimal strategy of investment in maintaining their bodies.


Abstract

The demonstration of lifespan plasticity in natural populations would provide a powerful test of evolutionary theories of senescence. Plastic senescence is not easily explained by mutation accumulation or antagonistic pleiotropy but is a corollary of the disposable soma theory. The lifespan differences among castes of the eusocial Hymenoptera are potentially some of the most striking and extreme examples of lifespan plasticity. Although these differences are often assumed to be plastic, this has never been demonstrated conclusively because differences in lifespan may be caused by the proximate effects of different levels of environmental hazard experienced by castes. Here, age-dependent and age-independent components of instantaneous mortality rates of the honeybee (Apis mellifera) were estimated from published lifetables for natural and semi-natural populations to determine whether differences in lifespan between queens and workers and between different types workers are indeed plastic. These differences in lifespan were found to be due to differences in the rate of actuarial senescence, which correlate positively with the rate of extrinsic mortality, in accordance with the central prediction of evolutionary theories of senescence. Although all three evolutionary theories of senescence could, in principle, explain such plastic senescence, given differential gene expression between castes or life stages, only the disposable soma theory adequately explains the adaptive regulation of somatic maintenance in response to different environmental conditions that appears to underlie lifespan plasticity.