scholarly journals Transcriptomic analyses of the termite, Cryptotermes secundus, reveal a gene network underlying a long lifespan and high fecundity

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Silu Lin ◽  
Jana Werle ◽  
Judith Korb

AbstractOrganisms are typically characterized by a trade-off between fecundity and longevity. Notable exceptions are social insects. In insect colonies, the reproducing caste (queens) outlive their non-reproducing nestmate workers by orders of magnitude and realize fecundities and lifespans unparalleled among insects. How this is achieved is not understood. Here, we identified a single module of co-expressed genes that characterized queens in the termite species Cryptotermes secundus. It encompassed genes from all essential pathways known to be involved in life-history regulation in solitary model organisms. By manipulating its endocrine component, we tested the recent hypothesis that re-wiring along the nutrient-sensing/endocrine/fecundity axis can account for the reversal of the fecundity/longevity trade-off in social insect queens. Our data from termites do not support this hypothesis. However, they revealed striking links to social communication that offer new avenues to understand the re-modelling of the fecundity/longevity trade-off in social insects.

2021 ◽  
Vol 376 (1823) ◽  
pp. 20190727
Author(s):  
Judith Korb ◽  
Jürgen Heinze

Individual lifespans vary tremendously between and also within species, but the proximate and ultimate causes of different ageing speeds are still not well understood. Sociality appears to be associated with the evolution of greater longevity and probably also with a larger plasticity of the shape and pace of ageing. For example, reproductives of several termites and ants reach lifespans that surpass those of their non-reproductive nestmates by one or two decades. In this issue, 15 papers explore the interrelations between sociality and individual longevity in both, group-living vertebrates and social insects. Here, we briefly give an overview of the contents of the various contributions, including theoretical and comparative studies, and we explore the similarities and dissimilarities in proximate mechanisms underlying ageing among taxa, with particular emphasis on nutrient-sensing pathways and, in insects, juvenile hormone. These studies point to an underestimated role of more downstream processes. We highlight the need for reliable transcriptomic markers of ageing and a comprehensive ageing theory of social animals, which includes the reproductive potential of workers, and considers the fact that social insect queens reach maturity only after a prolonged period of producing non-reproductive workers. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’


2021 ◽  
Vol 376 (1823) ◽  
pp. 20190728 ◽  
Author(s):  
Judith Korb ◽  
Karen Meusemann ◽  
Denise Aumer ◽  
Abel Bernadou ◽  
Daniel Elsner ◽  
...  

The exceptional longevity of social insect queens despite their lifelong high fecundity remains poorly understood in ageing biology. To gain insights into the mechanisms that might underlie ageing in social insects, we compared gene expression patterns between young and old castes (both queens and workers) across different lineages of social insects (two termite, two bee and two ant species). After global analyses, we paid particular attention to genes of the insulin/insulin-like growth factor 1 signalling (IIS)/target of rapamycin (TOR)/juvenile hormone (JH) network, which is well known to regulate lifespan and the trade-off between reproduction and somatic maintenance in solitary insects. Our results reveal a major role of the downstream components and target genes of this network (e.g. JH signalling, vitellogenins, major royal jelly proteins and immune genes) in affecting ageing and the caste-specific physiology of social insects, but an apparently lesser role of the upstream IIS/TOR signalling components. Together with a growing appreciation of the importance of such downstream targets, this leads us to propose the TI–J–LiFe ( T OR/ I IS– J H– Li fespan and Fe cundity) network as a conceptual framework for understanding the mechanisms of ageing and fecundity in social insects and beyond. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’


2021 ◽  
Vol 376 (1823) ◽  
pp. 20190739 ◽  
Author(s):  
Veronika Rau ◽  
Judith Korb

Social insects seem to have overcome the almost universal trade-off between fecundity and longevity as queens can be highly fecund and at the same time reach lifespans of decades. By contrast, their non-reproducing workers are often short-lived. One hypothesis to explain the long lifespan of queens is that they are better protected against stress than their workers. However, evidence is controversial and experimental studies are scarce. We aimed at manipulating environmental stress and ageing by exposing colonies of the less-socially complex termite Cryptotermes secundus to temperature regimes that differed in variance. In contrast with expectation, constant temperatures imposed more stress than variable temperatures. Survival of queens and workers as well as queens' fecundity were partly reduced under constant conditions and both castes showed signs of ageing in the transcriptome signature under constant conditions. There was a clear oxidative stress defence signal under constant conditions that was, surprisingly, stronger for workers than queens. We discuss how our results relate to social complexity. We argue that workers that are totipotent to become reproductives, like in C. secundus , should invest more in ‘anti-ageing' mechanisms than sterile workers because the former can still reproduce and have not reached maturity yet. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’


2018 ◽  
Vol 285 (1892) ◽  
pp. 20182141 ◽  
Author(s):  
Stefania Casagrande ◽  
Michaela Hau

The trade-off between reproductive investment and survival is central to life-history theory, but the relative importance and the complex interactions among the physiological mechanisms mediating it are still debated. Here we experimentally tested whether baseline glucocorticoid hormones, the redox system or their interaction mediate reproductive investment–survival trade-offs in wild great tits ( Parus major ). We increased the workload of parental males by clipping three feathers on each wing, and 5 days later determined effects on baseline corticosterone concentrations (Cort), redox state (reactive oxygen metabolites, protein carbonyls, glutathione peroxidase [GPx], total non-enzymatic antioxidants), body mass, body condition, reproductive success and survival. Feather-clipping did not affect fledgling numbers, chick body condition, nest provisioning rates or survival compared with controls. However, feather-clipped males lost mass and increased both Cort and GPx concentrations. Within feather-clipped individuals, GPx increases were positively associated with reproductive investment (i.e. male nest provisioning). Furthermore, within all individuals, males that increased GPx suffered reduced survival rates. Baseline Cort increases were related to mass loss but not to redox state, nest provisioning or male survival. Our findings provide experimental evidence that changes in the redox system are associated with the trade-off between reproductive investment and survival, while baseline Cort may support this trade-off indirectly through a link with body condition. These results also emphasize that plastic changes in individuals, rather than static levels of physiological signals, may mediate life-history trade-offs.


Author(s):  
Stefan Wötzel ◽  
Marco Andrello ◽  
Maria Albani ◽  
Marcus Koch ◽  
George Coupland ◽  
...  

Many model organisms have obtained a prominent status due to an advantageous combination of their life-history characteristics, genetic properties and also practical considerations. In non-crop plants, Arabidopsis thaliana is the most renowned model and has been used as study system to elucidate numerous biological processes at the molecular level. Once a complete genome sequence was available, research has markedly accelerated and further established A. thaliana as the reference to stimulate studies in other species with different biology. Within the Brassicaceae family, the arctic-alpine perennial Arabis alpina has become a model complementary to A. thaliana to study life-history evolution and ecological genomics in harsh environments. In this review, we provide an overview of the properties that facilitated the rapid emergence of A. alpina as a plant model. We summarize the evolutionary history of A. alpina, including the diversification of its mating system, and discuss recent progress in the molecular dissection of developmental traits that are related to its perennial life history and environmental adaptation. We indicate open questions from which future research might be developed in other Brassicaceae species or more distantly related plant families.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Adria C LeBoeuf ◽  
Patrice Waridel ◽  
Colin S Brent ◽  
Andre N Gonçalves ◽  
Laure Menin ◽  
...  

Social insects frequently engage in oral fluid exchange – trophallaxis – between adults, and between adults and larvae. Although trophallaxis is widely considered a food-sharing mechanism, we hypothesized that endogenous components of this fluid might underlie a novel means of chemical communication between colony members. Through protein and small-molecule mass spectrometry and RNA sequencing, we found that trophallactic fluid in the ant Camponotus floridanus contains a set of specific digestion- and non-digestion related proteins, as well as hydrocarbons, microRNAs, and a key developmental regulator, juvenile hormone. When C. floridanus workers’ food was supplemented with this hormone, the larvae they reared via trophallaxis were twice as likely to complete metamorphosis and became larger workers. Comparison of trophallactic fluid proteins across social insect species revealed that many are regulators of growth, development and behavioral maturation. These results suggest that trophallaxis plays previously unsuspected roles in communication and enables communal control of colony phenotypes.


2021 ◽  
Vol 9 ◽  
Author(s):  
Abel Bernadou ◽  
Boris H. Kramer ◽  
Judith Korb

The evolution of eusociality in social insects, such as termites, ants, and some bees and wasps, has been regarded as a major evolutionary transition (MET). Yet, there is some debate whether all species qualify. Here, we argue that worker sterility is a decisive criterion to determine whether species have passed a MET (= superorganisms), or not. When workers are sterile, reproductive interests align among group members as individual fitness is transferred to the colony level. Division of labour among cooperating units is a major driver that favours the evolution of METs across all biological scales. Many METs are characterised by a differentiation into reproductive versus maintenance functions. In social insects, the queen specialises on reproduction while workers take over maintenance functions such as food provisioning. Such division of labour allows specialisation and it reshapes life history trade-offs among cooperating units. For instance, individuals within colonies of social insects can overcome the omnipresent fecundity/longevity trade-off, which limits reproductive success in organisms, when increased fecundity shortens lifespan. Social insect queens (particularly in superorganismal species) can reach adult lifespans of several decades and are among the most fecund terrestrial animals. The resulting enormous reproductive output may contribute to explain why some genera of social insects became so successful. Indeed, superorganismal ant lineages have more species than those that have not passed a MET. We conclude that the release from life history constraints at the individual level is a important, yet understudied, factor across METs to explain their evolutionary success.


2012 ◽  
Vol 279 (1744) ◽  
pp. 4033-4041 ◽  
Author(s):  
J. Vézilier ◽  
A. Nicot ◽  
S. Gandon ◽  
A. Rivero

Long-lived mosquitoes maximize the chances of Plasmodium transmission. Yet, in spite of decades of research, the effect of Plasmodium parasites on mosquito longevity remains highly controversial. On the one hand, many studies report shorter lifespans in infected mosquitoes. On the other hand, parallel (but separate) studies show that Plasmodium reduces fecundity and imply that this is an adaptive strategy of the parasite aimed at redirecting resources towards longevity. No study till date has, however, investigated fecundity and longevity in the same individuals to see whether this prediction holds. In this study, we follow for both fecundity and longevity in Plasmodium- infected and uninfected mosquitoes using a novel, albeit natural, experimental system. We also explore whether the genetic variations that arise through the evolution of insecticide resistance modulate the effect of Plasmodium on these two life-history traits. We show that (i) a reduction in fecundity in Plasmodium- infected mosquitoes is accompanied by an increase in longevity; (ii) this increase in longevity arises through a trade-off between reproduction and survival; and (iii) in insecticide-resistant mosquitoes, the slope of this trade-off is steeper when the mosquito is infected by Plasmodium (cost of insecticide resistance).


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