The co‐evolution of longevity and social life

Lucas, Eric R.; Keller, Laurent

doi:10.1111/1365-2435.13445

Cited by 60 publications

(88 citation statements)

References 102 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…The analysis of the interaction between the immune challenge and fertility revealed that fertile workers invest more into molecular repair mechanisms such as telomere maintenance , base-excision repair and nucleotide-excision repair than infertile workers. Since telomere maintenance and DNA damage repair systems are strong predictors of lifespan [ 8 , 53 , 54 ], our findings indicate that fertile workers invest more into somatic maintenance, which could well explain their extended lifespan. Our results show weak changes in the expression of fertility genes in the fat body, indicating that this tissue plays a lesser role in the molecular regulation of fertility.…”

Section: Discussionmentioning

confidence: 84%

Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect

et al. 2020

View full text Add to dashboard Cite

Background The gut microbiome can influence life history traits associated with host fitness such as fecundity and longevity. In most organisms, these two life history traits are traded-off, while they are positively linked in social insects. In ants, highly fecund queens can live for decades, while their non-reproducing workers exhibit much shorter lifespans. Yet, when fertility is induced in workers by death or removal of the queen, worker lifespan can increase. It is unclear how this positive link between fecundity and longevity is achieved and what role the gut microbiome and the immune system play in this. To gain insights into the molecular regulation of lifespan in social insects, we investigated fat body gene expression and gut microbiome composition in workers of the ant Temnothorax rugatulus in response to an experimental induction of fertility and an immune challenge. Results Fertile workers upregulated several molecular repair mechanisms, which could explain their extended lifespan. The immune challenge altered the expression of several thousand genes in the fat body, including many immune genes, and, interestingly, this transcriptomic response depended on worker fertility. For example, only fertile, immune-challenged workers upregulated genes involved in the synthesis of alpha-ketoglutarate, an immune system regulator, which extends the lifespan in Caenorhabditis elegans by down-regulating the TOR pathway and reducing oxidant production. Additionally, we observed a dramatic loss in bacterial diversity in the guts of the ants within a day of the immune challenge. Yet, bacterial density did not change, so that the gut microbiomes of many immune challenged workers consisted of only a single or a few bacterial strains. Moreover, the expression of immune genes was linked to the gut microbiome composition, suggesting that the ant host can regulate the microbiome in its gut. Conclusions Immune system flare-ups can have negative consequence on gut microbiome diversity, pointing to a previously underrated cost of immunity. Moreover, our results provide important insights into shifts in the molecular regulation of fertility and longevity associated with insect sociality.

show abstract

Section: Discussionmentioning

confidence: 84%

Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect

et al. 2020

View full text Add to dashboard Cite

show abstract

“…Comparative studies of birds and insects have shown that species with cooperative and eusocial breeding systems have extended lifespans (Arnold & Owens, 1998;Downing, Cornwallis & Griffin, 2015;Keller & Genoud, 1997;Keller, 1998;Beauchamp, 2014). A common explanation for the association between these breeding systems and increased lifespan is that group-living reduces the extrinsic mortality of breeding individuals, which selects for greater longevity (Lucas & Keller, 2019). This is thought to be the case in eusocial insect societies where the 'queens' of many ant, bee and termite species live in a sheltered nest that is defended against predators by a large workforce (Carey, 2001;Hölldobler & Wilson, 1990).…”

Section: Introductionmentioning

confidence: 99%

“…In this study, we re-visit the question of whether sociality, fossoriality, or both, are related to increases in maximum lifespan. The intention is not to detract from the results of the previous studies, but to place these results in context, as the ongoing reference to a link between sociality and increased lifespan in mammals (Downing, Cornwallis & Griffin, 2015;Lucas & Keller, 2019) could give the perception of a robust and resolved trend in spite of an equivocal evidence base. Indeed, not all published studies have demonstrated a positive effect of cooperative breeding on maximum lifespan.…”

Section: Introductionmentioning

confidence: 99%

The case for extended lifespan in cooperatively breeding mammals: a re-appraisal

Thorley¹

2020

PeerJ

View full text Add to dashboard Cite

Recent comparative studies have suggested that cooperative breeding is associated with increases in maximum lifespan among mammals, replicating a pattern also seen in birds and insects. In this study, we re-examine the case for increased lifespan in mammalian cooperative breeders by analysing a large dataset of maximum longevity records. We did not find any consistent, strong evidence that cooperative breeders have longer lifespans than other mammals after having controlled for variation in body mass, mode of life and data quality. The only possible exception to this general trend is found in the African mole-rats (the Bathyergid family), where all members are relatively long-lived, but where the social, cooperatively breeding species appear to be much longer-lived than the solitary species. However, solitary mole-rat species have rarely been kept in captivity or followed longitudinally in the wild and so it seems likely that their maximum lifespan has been underestimated when compared to the highly researched social species. Although few subterranean mammals have received much attention in a captive or wild setting, current data instead supports a causal role of subterranean living on lifespan extension in mammals.

show abstract

“…Sociality is evolutionarily associated with a complex set of life-history traits. Most notably, social species might have longer lifespan and decreased actuarial senescence (see [7–9] for reviews). Indeed, social life in cooperative breeders and colonial species can buffer environmentally-driven mortality risks and might ultimately slow down actuarial senescence (e.g.…”

Section: Introductionmentioning

confidence: 99%

Is degree of sociality associated with reproductive senescence? A comparative analysis across birds and mammals

Vágási

Vincze

Lemaître

et al. 2020

Preprint

View full text Add to dashboard Cite

Our understanding on how widespread reproductive senescence is in the wild and how the onset and rate of reproductive senescence vary among species in relation to life histories and lifestyles is currently limited. More specifically, whether the species-specific degree of sociality is linked to the occurrence, onset and rate of reproductive senescence remains unknown. Here, we investigate these questions using phylogenetic comparative analyses across 36 bird and 101 mammal species encompassing a wide array of life histories, lifestyles and social traits. We found that female reproductive senescence (1) is widespread and occurs with similar frequency (about two thirds) in birds and mammals; (2) occurs later in life and is slower in birds than in similar-sized mammals; (3) occurs later in life and is slower with an increasingly slower pace of life in both vertebrate classes; and (4) is only weakly associated, if any, with the degree of sociality in both classes after accounting for the effect of body size and pace of life. However, when allowing for species differences in pace of life, a higher degree of sociality was associated with later and weaker reproductive senescence in females, which suggests that degree of sociality is indirectly related to reproductive senescence via the pace of life.Subject Areasecology, evolution

show abstract

The co‐evolution of longevity and social life

Cited by 60 publications

References 102 publications

Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect

Immune challenge reduces gut microbial diversity and triggers fertility-dependent gene expression changes in a social insect

The case for extended lifespan in cooperatively breeding mammals: a re-appraisal

Is degree of sociality associated with reproductive senescence? A comparative analysis across birds and mammals

Contact Info

Product

Resources

About