Sex-specific patterns of senescence in artificial insect populations varying in sex-ratio to manipulate reproductive effort

Jehan, Charly; Chogne, Manon; Rigaud, Thierry; Moret, Yannick

doi:10.1186/s12862-020-1586-x

Cited by 15 publications

(19 citation statements)

References 84 publications

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“…The early life reproduction period corresponds to the age range during which all females are sexually mature and produce a large number of eggs (up to 30 eggs) per day (Dick, 1937;Drnevich et al, 2001). The late-life reproductive period corresponds to the age range during which survival is still high (above 95%, Jehan et al, 2020), preventing selective disappearance, and for which egg production is strongly declining. Indeed, from 40 to 60 days old, egg production is usually about one egg a day and negligible after 80 days old (Dick, 1937;Jehan et al, 2020).…”

Section: Insect Culture and Experimental Designmentioning

confidence: 99%

“…The late-life reproductive period corresponds to the age range during which survival is still high (above 95%, Jehan et al, 2020), preventing selective disappearance, and for which egg production is strongly declining. Indeed, from 40 to 60 days old, egg production is usually about one egg a day and negligible after 80 days old (Dick, 1937;Jehan et al, 2020).…”

Section: Insect Culture and Experimental Designmentioning

confidence: 99%

“…Haemocyte counts were found to decrease after mating (Fedorka et al, 2004;McKean & Nunney, 2001). Haemocyte numbers decline or remain unchanged with age, depending on the insect species studied (Adamo et al, 2001;Doums et al, 2002;Horn et al, 2014;Jehan et al, 2020). In addition, microbial challenge also induces the production of antibacterial peptides in the haemolymph (Vigneron et al, 2019), an energetically costly process that may reduce survival (Moret & Schmid-Hempel, 2000).…”

Section: Introductionmentioning

confidence: 99%

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Late‐life reproduction in an insect: Terminal investment, reproductive restraint or senescence

Jehan

Sabarly

Rigaud

et al. 2020

Journal of Animal Ecology

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1. The terminal investment, reproductive restraint or senescence theories may explain individual late-life patterns of reproduction. The terminal investment hypothesis predicts that individuals increase reproductive allocation late in life as prospects for future survival decrease. The other two hypotheses predict reduced reproduction late in life, but for different reasons. Under the Reproductive Restraint hypothesis, individuals restrain their reproductive effort to sustain future survival and gain more time for reproducing, whereas under the Senescence process, reproduction is constrained because of somatic deterioration. While these hypotheses imply that reproduction is costly, they should have contrasted implications in terms of survival after late reproduction and somatic maintenance. 2. Testing these hypotheses requires proper consideration of the effects of agedependent reproductive effort on post-reproduction survival and age-related somatic functions. We experimentally tested these three hypotheses in females of the mealworm beetle, Tenebrio molitor, an iteroparous and income breeder insect. We manipulated their age-specific allocation into reproduction and observed the effects of this manipulation on their late-life fecundity, post-reproduction survival and immunocompetence as a measurement of somatic protection. 3. We found that females exhibit age-related decline in fecundity and that this reproductive senescence is accelerated by a cost of early reproduction. The cost of reproduction had no significant effect on female longevity and their ability to survive a bacterial infection, despite that some immune cells were depleted by reproduction. We found that female post-infection survival deteriorated with age, which could be partly explained by a decline in some immune parameters. Importantly, females did not increase their reproductive effort late in life at the expense of their late-life post-reproduction survival. 4. Late-life reproduction in T. molitor females is senescing and not consistent with a terminal investment strategy. Rather, our results suggest that females allocate resources according to a priority scheme favouring longevity at the expense of reproduction, which is in line with the reproductive restraint hypothesis. 5. Such a priority scheme also shows that a relatively short-lived insect can evolve life-history strategies hitherto known only in long-lived animals. This puts in perspective the role of longevity in the evolution of life-history strategies.

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Section: Insect Culture and Experimental Designmentioning

confidence: 99%

Section: Insect Culture and Experimental Designmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Late‐life reproduction in an insect: Terminal investment, reproductive restraint or senescence

Jehan

Sabarly

Rigaud

et al. 2020

Journal of Animal Ecology

Self Cite

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“…Female fecundity declines after about 2 weeks but reproduction does not stop (Dick, 1937;Jehan et al, 2020). These features possibly allow females of this insect to adjust their lifetime reproductive effort according to variation in their physiological state and environmental conditions.…”

Section: Introductionmentioning

confidence: 98%

Age‐specific fecundity under pathogenic threat in an insect: Terminal investment versus reproductive restraint

Jehan

Sabarly

Rigaud

et al. 2021

Journal of Animal Ecology

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1. The terminal investment hypothesis predicts that as an organism's prospects for survival decrease, through age or when exposed to a pathogenic infection, it will invest more in reproduction, which should trade-off against somatic maintenance (including immunity) and therefore future survival. Attempts to test this hypothesis have produced mixed results, which, in addition, mainly rely on the assessment of changes in reproductive effort and often overlooking its impact on somatic defences and survival. Alternatively, animals may restrain current reproduction to sustain somatic protection, increasing the chance of surviving for additional reproductive opportunities.2. We tested both of these hypotheses in females of the yellow mealworm beetle, Tenebrio molitor, an iteroparous insect with reproductive tactics similar to that of long-lived organisms.3. To achieve this, we mimicked pathogenic bacterial infections early or late in the life of breeding females by injecting them with a suspension of inactivated Bacillus cereus, a known natural pathogen of T. molitor, and measured female age-specific fecundity, survival, body mass and immunity.4. Inconsistent with a terminal investment, females given either an early or late-life immune challenge did not exhibit reduced survival or enhance their reproductive output. Female fecundity declined with age and was reduced by the early but not the late immune challenge. Both early and late-life fecundity correlated positively with life expectancy. Finally, young and old females exhibited similar antibacterial immune responses, suggesting that they both restrained reproduction to sustain immunity. 5. Our results clearly demonstrate that age-specific reproduction of T. molitor females under pathogenic threat is inconsistent with a terminal investment. In contrast, our results instead suggest that females used a reproductive restraint strategy to sustain immunity and therefore subsequent reproductive opportunities. However, as infections were mimicked only, the fitness benefit of this reproductive restraint could not be shown.

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“…From a selective point of view, increasing the copy number of many TE families might be beneficial for longevity, whereas only a small number of families may affect lifespan negatively. Although speculative, a higher TE abundance could result in an enhanced piRNA-production and a better protection from TEs, thereby improving survival ( Jones et al 2016 ; Luo et al 2020 ). Under this scenario, selection would likely lead to parallel increases or decreases of the same TE families across studies.…”

Section: Discussionmentioning

confidence: 99%

Transposable Element Landscape in Drosophila Populations Selected for Longevity

Fabian

Dönertaş

Fuentealba

et al. 2021

Genome Biology and Evolution

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Transposable elements (TEs) inflict numerous negative effects on health and fitness as they replicate by integrating into new regions of the host genome. Even though organisms employ powerful mechanisms to demobilize TEs, transposons gradually lose repression during aging. The rising TE activity causes genomic instability and was implicated in age-dependent neurodegenerative diseases, inflammation and the determination of lifespan. It is therefore conceivable that long-lived individuals have improved TE silencing mechanisms resulting in reduced TE expression relative to their shorter-lived counterparts and fewer genomic insertions. Here, we test this hypothesis by performing the first genome-wide analysis of TE insertions and expression in populations of Drosophila melanogaster selected for longevity through late-life reproduction for 50-170 generations from four independent studies. Contrary to our expectation, TE families were generally more abundant in long-lived populations compared to non-selected controls. Although simulations showed that this was not expected under neutrality, we found little evidence for selection driving TE abundance differences. Additional RNA-seq analysis revealed a tendency for reducing TE expression in selected populations, which might be more important for lifespan than regulating genomic insertions. We further find limited evidence of parallel selection on genes related to TE regulation and transposition. However, telomeric TEs were genomically and transcriptionally more abundant in long-lived flies, suggesting improved telomere maintenance as a promising TE-mediated mechanism for prolonging lifespan. Our results provide a novel viewpoint indicating that reproduction at old age increases the opportunity of TEs to be passed on to the next generation with little impact on longevity.

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Sex-specific patterns of senescence in artificial insect populations varying in sex-ratio to manipulate reproductive effort

Cited by 15 publications

References 84 publications

Late‐life reproduction in an insect: Terminal investment, reproductive restraint or senescence

Late‐life reproduction in an insect: Terminal investment, reproductive restraint or senescence

Age‐specific fecundity under pathogenic threat in an insect: Terminal investment versus reproductive restraint

Transposable Element Landscape in Drosophila Populations Selected for Longevity

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