A unified framework for evolutionary genetic and physiological theories of aging

Lemaître, Jean-François; Moorad, Jacob; Gaillard, Jean-Michel; Maklakov, Alexei A.; Nussey, Daniel H.

doi:10.1371/journal.pbio.3002513

Cited by 16 publications

(3 citation statements)

References 97 publications

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“…Trade-offs among these three fundamental aspects of an organism's life play key roles in dictating the evolution of reproductive schedules, with cascading effects on organismal ageing and demography [3][4][5]. Indeed, some species invest heavily in early reproduction at the expense of longevity, while others prioritize growth and survival before reproducing, and these alternative strategies are expected outcomes of differences in mortality risk and age-related changes in the strength of natural selection [1,2,6].…”

Section: Introductionmentioning

confidence: 99%

Coevolution of longevity and female germline maintenance

Baur,

Koppik,

Savković

et al. 2024

Proc. R. Soc. B.

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An often-overlooked aspect of life-history optimization is the allocation of resources to protect the germline and secure safe transmission of genetic information. While failure to do so renders significant fitness consequences in future generations, germline maintenance comes with substantial costs. Thus, germline allocation should trade off with other life-history decisions and be optimized in accordance with an organism’s reproductive schedule. Here, we tested this hypothesis by studying germline maintenance in lines of seed beetle, selected for early (E) or late (L) reproduction for 350 and 240 generations, respectively. Female animals provide maintenance and screening of male gametes in their reproductive tract and oocytes. Here, we reveal the ability of young and aged E- and L-females to provide this form of germline maintenance by mating them to males with ejaculates with artificially elevated levels of protein and DNA damage. We find that germline maintenance in E-females peaks at young age and then declines, while the opposite is true for L-females, in accordance with the age of reproduction in the respective regime. These findings identify the central role of allocation to secure germline integrity in life-history evolution and highlight how females can play a crucial role in mitigating the effects of male germline decisions on mutation rate and offspring quality.

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Section: Introductionmentioning

confidence: 99%

Coevolution of longevity and female germline maintenance

Baur,

Koppik,

Savković

et al. 2024

Proc. R. Soc. B.

View full text Add to dashboard Cite

show abstract

“…Trade-offs among these three fundamental aspects of an organism's life play key roles in dictating the evolution of reproductive schedules, with cascading effects on organismal aging and demography (3)(4)(5). Indeed, some species invest heavily in early reproduction at the expense of longevity, while others prioritize growth and survival before reproducing, and these alternative strategies are expected outcomes of differences in mortality risk and age-related changes in the strength of natural selection (1,2,6).…”

Section: Introductionmentioning

confidence: 99%

Coevolution of longevity and female germline maintenance

Baur,

Koppik,

Savkovic

et al. 2023

Preprint

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An often-overlooked aspect of life-history optimization is the allocation of resources to protect the germline and secure safe transmission of genetic information. While failure to do so renders significant fitness consequences in future generations, germline maintenance comes with substantial costs. Thus, germline allocation should trade-off with other life history decisions and be optimized in accord with an organism’s reproductive schedule. Here we tested this hypothesis by studying germline maintenance in lines of seed beetle, selected for early (E) or late (L) reproduction for 350 and 240 generations, respectively. Female animals provide maintenance of male gametes in their reproductive tract and oocytes. Here, we revealed the ability of young and old E and L-females to provide this form of germline maintenance by mating them to males with ejaculates with artificially elevated levels of protein and DNA damage. We find pronounced evolved differences in this form of germline maintenance between E and L females that accord with the age of reproduction in respective regime. These findings identify the central role of allocation to secure germline integrity in life history evolution and highlight how females can play a crucial role in mitigating effects of male germline decisions on mutation rate and offspring quality.

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“…Obligate asexual planaria do not show physiological senescence (Sahu et al, 2017). In these animals, stem cells also function as germ line, and so many of the well-known somatic mechanisms of senescence (Finkel & Holbrook, 2000;Lemaître et al, 2024;Payne & Chinnery, 2015) do not apply to obligate asexual planarian stem cells (Sahu et al, 2017). However, individuals of planarians can still suffer suboptimal conditions of stress, shrink, and even die (e.g., Ofoegbu et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Non-senescent species are not immortal: stress and decline in two planaria species

Deere

Holland

Aboobaker

et al. 2023

Preprint

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The impacts of resource availability on senescence, the loss of vitality with age, are formalised under the Calorie Restriction (CR) theory, which predicts that the onset of senescence is delayed and life expectancy prolonged due to the ultimate effects of restricted resource intake without malnutrition. However, CR studies are largely implemented in unrealistic environments that do not consider how interacting, stochastic drivers impact longevity. Indeed, little is known about the impact of stochastic resource availability on senescence, even though environmental stochasticity is the norm rather than an exception in natural populations. Here, we examine whether and how stochasticity in the quantity, quality, and frequency of resources impact lifespan, life history trait trade-offs, and population structure in two long-lived planaria: Schmidtea mediterranea and Dugesia tahitiensis. For each species, we estimate weekly population size, survival, and a size distribution metric that quantifies population structure and skew. Over the 19-week study, survival in S. mediterranea is lower than D. tahitiensis across all feeding regimes. However, for both species, CR does not diminish survival. There are also no clear shifts in population structure over time across the different feeding regimes. For S. mediterranea, in most treatments, population structure changed to fewer smaller than larger individuals (right-skewed). In the case of D. tahitiensis, only treatments where resources are provided frequently cause right-skewed population structures. Population size also varied between species, with that of D. tahitiensis never declining across treatments, and always becoming larger than S. mediterranea; in the case of S. mediterranea, most treatments show a decline in population counts over the study period. As before, no clear pattern emerges in the changes in population counts under CR conditions for both species. As such, we did not find evidence of CR providing benefits in terms of lifespan nor trade-off between population counts, survival, and body size. We call for the careful re-evaluation of decades of CR work in short-lived species, by expanding and testing predictions in more realistic settings and across a wider range of life histories.

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A unified framework for evolutionary genetic and physiological theories of aging

Cited by 16 publications

References 97 publications

Coevolution of longevity and female germline maintenance

Coevolution of longevity and female germline maintenance

Coevolution of longevity and female germline maintenance

Non-senescent species are not immortal: stress and decline in two planaria species

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