Life history evolution and ageing in termites
Evolution, Anthropology
Final Report Abstract
Almost all animals age but they do so at different pace. So why can some animals live for many decades and others only for a few days? Social insects offer promising new avenues for ageing research. Within ant and termite colonies we find some of the most long-lived insects, the reproductives (queens and in termites also kings) that can have lifespans of more than 20 years. At the same time, the non-reproducing workers often live a few months only, although they share the same genetic background. This pattern also seems to contradict the common life history trade-off that an increased fecundity reduces longevity. In this project we investigated why (ultimate causes) and how (proximate mechanisms) social insect queens can live so long and apparently overcome the fecundity/longevity trade-off. We used the drywood termite Cryptotermes secundus as model organism. This species lives in socially less complex colonies of a few hundred individuals where workers are totipotent to develop into reproductives. By experimentally increasing the fecundity of queens we could demonstrate that queens indeed seem to have overcome the fecundity/longevity trade-off as they did not suffer from increased mortality and also their future fecundity seemed unaffected. However, workers suffered and had reduced survival. They fed the queen more under increased fecundity conditions. Our results suggest that workers take over the queen’s burden. Hence, the tradeoff seems shifted from within an individual (the queen) to other colony members (the workers). Our gene expression and genomic analyses suggest that changes along the IIS-FOXO-JH axis (insulin/insulin-like growth factor 1 signalling - forkhead box O transcritpion factor - juvenile hormone; i.e. central regulators of fecundity and longevity) may mechanistically explain how queens have overcome the fecundity/longevity trade-off. Like most solitary insects - including cockroaches to which termites belong - reproducing queens are characterised by an upregulation of the IIS pathway and high JH titres which are linked to oogenesis. However, this upregulation of the IIS pathway does not result in the typical inhibition of the transcription factor FOXO, but instead activates it. As FOXO generally functions as an ‘anti-ageing factor’, this could explain how these termite queens can be highly fecund and at the same time live very long. Finally, our transcriptome analyses that compared young and old individuals, revealed that old reproductives do show a few signs of ageing while workers also seem to invest in antiageing mechanisms. This is in line with predictions of life history theory: Ageing is expected to start after reaching maturity and C. secundus workers are immatures that have not reached maturity yet. Overall, our project provided new insights into the proximate mechanisms and ultimate causes underlying ageing. Given that the mechanisms of ageing are highly conserved among taxa, our results might also contribute to improve our understanding of ageing in mammals, including humans.
Publications
- (2016) Social insects: aging and the re-shaping of the fecundity/longevity trade-off. Current Opinion in Insect Science 16:1-4
Monroy Kuhn JM, Korb J
(See online at https://doi.org/10.1016/j.cois.2016.06.002) - (2016) Why do social insect queens live so long? Approaches to unravel the socialityaginng puzzle. Current Opinion in Insect Science 16:104-107
Korb J
(See online at https://doi.org/10.1016/j.cois.2016.06.004) - (2018) Hemimetabolous genomes reveal molecular basis of termite eusociality. Nature Ecology and Evolution 2:e 557
Harrison MC, et al. ... Korb J, Bornberg-Bauer E
(See online at https://doi.org/10.1038/s41559-017-0459-1) - (2018) Reconstructed evolution of insulin receptors in insects reveals duplications in early insects and cockroaches. Journal of Experimental Zoology (Mol Dev Evol) 330:305-311
Kremer LPM, Korb J, Bornberg-Bauer E
(See online at https://doi.org/10.1002/jez.b.22809) - (2018) Remodeling of the juvenile hormone pathway through caste-biased gene expression and positive selection along a gradient of termite eusociality. Journal of Experimental Zoology (Mol Dev Evol) 330:296-304
Jongepier E, Kemena C, Lopez-Ezquerra A, Belles X, Bornberg-Bauer E, Korb J
(See online at https://doi.org/10.1002/jez.b.22805) - (2019) Long live the queen, the king and the commoner? Transcript expression differences between old and young in the termite Cryptotermes secundus. PLoS One 14:e0210371
Monroy Kuhn JM, Meusemann K, Korb J
(See online at https://doi.org/10.1371/journal.pone.0210371)
