Longevity of insects with social castes

From Longevity Wiki

Social insects such as ants,[1] bees,[2] and termites,[3] have a distinct division of labor among individuals within their colonies. The colony is typically composed of a reproductive queen or queens and non-reproductive workers or soldier castes.[4] Research has shown that there are significant differences in longevity between the queen and worker castes in many social insect species. In general, queens live much longer than workers, and any worker can become a queen given the appropriate environmental cues by turning on or off specific genes (i.e. via epigenetic mechanisms).[5]

The difference in longevity of the social castes is thought to be related to the different roles that queens and workers play within the colony. Queens are responsible for reproducing and maintaining the colony, so they have evolved to live longer in order to increase their chances of reproducing.[6] In contrast, workers are responsible for foraging food and caring for the colony's young, so they have evolved to have shorter lifespans as they expend a lot of energy and are more prone to injuries and predation.[6] Additionally, queen ants and bees have a different hormonal regulation that allows them to live longer, and different gene expression profiles that increases their resistance to stress, while reducing their metabolism.

The fact that queens live many times longer than workers, despite sharing the same genome, provides a particularly useful model for understanding the epigenetic pathways and mechanisms that influence aging.[5]

Longevity of workers and queens

Bees

Laying worker bee.[7]

In hives, queen bees are normally the only female who reproduces, whereas the vast majority of bees are sterile females known as worker bees. Queen honeybees can live for several years, while workers typically only live for several months.[6]

Even in a normal hive, about 1% of workers have ovaries developed enough to lay eggs. A laying worker bee is a worker bee that lays unfertilized eggs, usually in the queenless colonies. In colonies of the neotropical stingless bee Scaptotrigona aff. postica, the lifespan of worker bees was about a third longer in hives without mated queens (known as non-queenright colonies).[8]

The worker bees of this species substantially alter their behavior without mated queens, for example by spending more time inside the nest building brood cells rather than participating in more risky foraging behaviors, therefore causing an increase in their overall longevity. Workers also start to lay haploid eggs, allowing some direct reproduction by workers in the absence of a queen.[8] This phenomenons highlight the plasticity of longevity in honeybees depending on environmental stimuli.

Ants

Gamergate worker ant. Gamergates are worker ants that reproduce sexually and lay fertilized eggs that will develop as females.

Ants also display a remarkable plasticity in their longevity that can be regulated via epigenetic mechanisms.[5] For instance, in the ant species L. niger, queen ants live for 20 to 30 years, workers for 1 to 3 years and males for only a few weeks.[9]

Gamergate ants

While in most ant species social castes are permanently established during the larval stage, adult Harpegnathos saltator workers can acquire a queen-like phenotype and become reproductive individuals called “gamergates”.[10] Workers that become gamergates also attain queen-like longevity, with a fivefold increase in average life span from 7 months to 3 years.[11]

In the ant Harpegnathos saltator, aging workers exhibited a progressive loss of ensheathing glia cells, whereas in gamergates, they remained a larger proportion of total glia cells over the same time span. Consistent with this, old gamergates retained the ability to mount a response to neuronal damage, which was lost in old workers.[12]

It was found that gamergates have elevated expression of gamergate-specific gene encoding a truncated form of a heat shock factor (HSF) most similar to mammalian HSF2 (hsalHSF2). In workers, hsalHSF2 was bound to DNA only upon heat stress, whereas in gamergates, hsalHSF2 bound to DNA even in the absence of heat stress and was localized to gamergate-biased heat shock response (HSR) genes. Expression of hsalHSF2 in Drosophila melanogaster led to enhanced heat shock survival and extended life span in the absence of heat stress.[13]

Tapeworm-infected ants
Tapeworm-infected ant workers.[14]

Parasite infection induces multiple alterations in the adult workers. After infection, the survival of infected workers is increased compared to their uninfected nest-mates.[15] [16] A parasitic tapeworm greatly lengthens the lives of its ant hosts by secreting a rich cocktail (more than 250 proteins) of antioxidants and other compounds.

Most secreted proteins from these parasitic tapeworms don't have any known annotated orthologs, which is indicative of potential novel functions and a long history of adaptation within this species interaction.[17]

A study found that both queens and infected workers express more of a gene called silver (carboxypeptidase D), compared to uninfected workers.[16] Researchers previously linked the silver gene to an extended lifespan in fruit flies.[18][19] However, a possible bias could be that infected workers do not engage in foraging outside the nest, and therefore have lower extrinsic mortality similar to queens, which also stay inside the nest.[16]

Wolbachia-infected ants
Pharaoh ants, a worker (left) and queen (right).[20]

Wolbachia, a widespread maternally-inherited endosymbiotic bacteria, infects an estimated one-third of all ant species. In infected Monomorium pharaonis colonies, queens produce more eggs. Despite increased egg-laying by queens and higher colony-level metabolic rates, Wolbachia infection was not associated with decreased queen lifespan. In fact, in workers, which are obligately sterile, Wolbachia infection was associated with longer lifespan.[21] Thus, increased egg-laying rates by queens and longer worker lifespans contribute to the higher growth rate and productivity that characterizes Wolbachia-infected colonies.

A role of metabolic provisioning of the host by endosymbionts has been demonstrated in several empirical studies. For example, Wolbachia can increase female fecundity in Drosophila flies by influencing iron homeostasis. In filarial nematodes, Wolbachia provisions the host with heme and riboflavin. Likewise, in a spider species, synthesis of fat and free amino acids has been shown to be improved by a Wolbachia infection, and in bedbugs, Wolbachia plays a nutritional role in vitamin B synthesis.[22][23]

Termites

Termites (Isoptera) are pale-coloured, soft-bodied eusocial insects living in complex societies that are characterized by a caste system in which despite the fact that all members in a termite colony have the same genetic background, few reproductively mature individuals (including a queen and a sperm-producing kings) reproduce and have extraordinarily long lives, while the large majority (non-reproductives, including workers and soldiers) perform tasks such as foraging, brooding and defence.[24][25] Unlike hymenopteran social insects (ants, bees and wasps), where the sterile workers are all female, in termites both males and females can be workers.[26] Furthermore, workers have unique flexibility in that a worker has the capability to develop into apterous neotenic reproductives that develop in the absence of reproductives to provide for continued growth of the colony.[27]

[28]

Although the question of how termite queens, which exhibit (as well as ants and honeybees) extraordinary longevity and fertility in comparison with non-reproductive individuals has attracted much attention, the molecular mechanisms involved are not yet understood. [29] It has been hypothesized that the queens of the termite Reticulitermes speratus have high level of oxidative stress resistance and suffer lower levels of oxidative damage than non-reproductive workers, due to the a highly efficient antioxidant system. In particular, queens had two times higher catalase activity and more than seven times higher expression levels of the catalase gene RsCAT1 than workers. Queens also showed higher expression levels of the peroxiredoxin gene RsPRX6.[30]

An important antioxidant contributing to survival in termites is uric acid, which is reserved and used as a valuable nitrogen source. Uric acid was shown to be provided by workers to reproductive castes.[31][32] It was found that king- and queen-specific degradation of uric acid contributes to reproduction and longevity in the subterranean termite Reticulitermes speratus. The urate oxidase gene (RsUAOX), which catalyses the first step of nitrogen recycling from stored uric acid, was highly expressed in mature kings and queens, and upregulated with differentiation into neotenic kings/queens.[33]

[34][35]

The haploid genome sizes (C-values) of termites (Isoptera) ranged from 0.58 to 1.90 pg, (1pg = 978 Mb).[36]

[37]

Mechanisms of exceptional longevity

Some of the most prominent mechanisms thought to underly the extended longevity of queens are:

Endocrine signalling and insulin binding protein Imp-L2

Imaginal morphogenesis protein‐Late 2 (Imp-L2), a putative homolog of vertebrate insulin-like growth factor (IGF)-binding protein 7 (IGFBP7), counteracts insulin/IGF signalling (IIS) in Drosophila and is essential for starvation resistance.[38] It is known that genetic manipulations of pathway components that result in dampened IIS extend lifespan in worms, flies and mice, and ameliorate age-dependent functional decline in a FOXO-dependent manner.[39] Increased IMP-L2 levels in Drosophila similarly results in substantial lifespan extension.[40]

It is assumed that in the process of egg-laying, some ant queens produce Imp-L2, which suppresses the aging effects of insulin, so that they can consume all the additional food needed for their egg-laying without shortening their lives.[41] As is known, reducing the AKT (also known as Protein kinase B) branch of insulin signaling in the fat body and adipose tissue lengthens the life of Drosophila.[42] A study showed that strong AKT phosphorylation after insulin treatment was completely suppressed by Imp-L2.[41]

Oxidative stress resistance

Vitellogenin (Vtg or Vg) is an egg yolk precursor produced by nearly all egg-laying females species. It is a source of nutrient and has additional roles in the scavenging of reactive oxygen species (ROS).[43] The expression of vitellogenin (Vg) appears to be linked to the queens increased resistance to stress.[44] Bees with higher Vg levels had increased survival, while reducing the expression of Vg led to decreased lifespan. However, in queen honey bees, the expression of antioxidant genes is not necessarily increased nor is required for their long lifespan.[45]

Genes underlying the reproductive division of labor

For identifying differences in gene expression between queens and workers in eusocial insects pairs of the queen and worker RNA sequencing data were used to calculate the queen/worker ratio referred to as the QW ratio.[46] Meta-analysis of RNA-seq data revealed 20 genes with differential expression between queens and workers. Among these genes, vitellogenin and vitellogenin receptors, which are highly expressed in queens across many social insects. SPARC (secreted protein acidic and cysteine rich) was highly expressed in queens, and RSG7 (regulator of G protein signaling 7) was highly expressed in workers. In mice, SPARC promotes insulin secretion via down-regulation of regulator of G protein 4 (RGS4) expression in pancreatic β cells. Functional analyses of the 20 genes retrieved from massive datasets of a large number of eusocial species may reveal in the future key regulators of the reproductive division of labor and and multiple differences in life expectancy.

When workers leave the natal colony or a queen dies, the expression of stage-specific genes is induced in workers, which leads to the differentiation of workers to reproductives.[47] In particular the relative expression level of Ras in the isolated female workers (IWs) was 131-fold than that of the workers, which indicated that Ras was especially overexpressed in workers in the absence of queens for activation of the Ras-ERK signalling pathway to drive the ovary development of isolated workers.[47] It was suggested that the signal transduction along the Ras-MAPK pathway crucially controls the reproductive plasticity of the workers and short-lived individuals can become long-lived individuals by the transition of castes.[47]

Effective transposon regulation

For termites but not for hymenopterans, it was found that caste and age was associated with the expression of transposable elements (TEs). While sterile workers who live only weeks had substantially higher TE activity, TE expression did not increase with age in the fat body of queens, despite a sevenfold increase in overall gene expression, due to a significant upregulation of the piRNA-pathway in 20-year-old queens of Macrotermes natalensis.[48][49]

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