Predicting adult lifespan and lifetime reproductive success from early-life reproductive events

2020 ◽  
Vol 167 (10) ◽  
Author(s):  
Matthew J. Powers ◽  
Ryan J. Weaver ◽  
Kyle B. Heine ◽  
Geoffrey E. Hill
Author(s):  
Anke Kloock ◽  
Lena Peters ◽  
Charlotte Rafaluk-Mohr

In most animals, female investment in offspring production is greater than for males. Lifetime reproductive success (LRS) is predicted to be optimized in females through extended lifespans to maximize reproductive events by increased investment in immunity. Males, however, maximize lifetime reproductive success by obtaining as many matings as possible. In populations consisting of mainly hermaphrodites, optimization of reproductive success may be primarily influenced by gamete and resource availability. Microbe-mediated protection (MMP) is known to affect both immunity and reproduction, but whether sex influences the response to MMP remains to be explored. Here, we investigated the sex-specific differences in survival, behavior, and timing of offspring production between feminized hermaphrodite (female) and male Caenorhabditis elegans following pathogenic infection with Staphylococcus aureus with or without MMP by Enterococcus faecalis. Overall, female survival decreased with increased mating. With MMP, females increased investment into offspring production, while males displayed higher behavioral activity. MMP was furthermore able to dampen costs that females experience due to mating with males. These results demonstrate that strategies employed under pathogen infection with and without MMP are sex dependent.


2019 ◽  
Vol 28 (5) ◽  
pp. 1127-1137 ◽  
Author(s):  
Justin R. Eastwood ◽  
Michelle L. Hall ◽  
Niki Teunissen ◽  
Sjouke A. Kingma ◽  
Nataly Hidalgo Aranzamendi ◽  
...  

2019 ◽  
Vol 374 (1770) ◽  
pp. 20180114 ◽  
Author(s):  
Emma I. K. Vitikainen ◽  
Faye J. Thompson ◽  
Harry H. Marshall ◽  
Michael A. Cant

Kin selection theory defines the conditions for which altruism or ‘helping’ can be favoured by natural selection. Tests of this theory in cooperatively breeding animals have focused on the short-term benefits to the recipients of help, such as improved growth or survival to adulthood. However, research on early-life effects suggests that there may be more durable, lifelong fitness impacts to the recipients of help, which in theory should strengthen selection for helping. Here, we show in cooperatively breeding banded mongooses ( Mungos mungo ) that care received in the first 3 months of life has lifelong fitness benefits for both male and female recipients. In this species, adult helpers called ‘escorts’ form exclusive one-to-one caring relationships with specific pups (not their own offspring), allowing us to isolate the effects of being escorted on later reproduction and survival. Pups that were more closely escorted were heavier at sexual maturity, which was associated with higher lifetime reproductive success for both sexes. Moreover, for female offspring, lifetime reproductive success increased with the level of escorting received per se , over and above any effect on body mass. Our results suggest that early-life social care has durable benefits to offspring of both sexes in this species. Given the well-established developmental effects of early-life care in laboratory animals and humans, we suggest that similar effects are likely to be widespread in social animals more generally. We discuss some of the implications of durable fitness benefits for the evolution of intergenerational helping in cooperative animal societies, including humans. This article is part of the theme issue ‘Developing differences: early-life effects and evolutionary medicine’.


2021 ◽  
Author(s):  
Anke Kloock ◽  
Lena Peters ◽  
Charlotte Elizabeth Rafaluk-Mohr

In most animals, female investment in offspring production is greater than for males. Lifetime reproductive success (LRS) is predicted to be optimised in females through extended lifespans to maximise reproductive events. Extended lifespan can be achieved through increased investment in immunity. Males, however, maximise lifetime reproductive success by obtaining as many matings as possible. Microbe-mediated protection (MMP) is known to affect both immunity and reproduction, but whether the two sexes respond differently to the provision of MMP remains to be explored. Here, we investigated the sex-specific differences in host life history traits between female and male Caenorhabditis elegans following pathogenic infection with Staphylococcus aureus with or without MMP by Enterococcus faecalis. Overall, female survival decreased with increased mating. With MMP, females increased investment into offspring production, while males displayed higher behavioural activity. These results highlight the different strategies employed by the two sexes under pathogen infection with and without MMP.


2020 ◽  
Vol 117 (40) ◽  
pp. 24909-24919 ◽  
Author(s):  
Chelsea J. Weibel ◽  
Jenny Tung ◽  
Susan C. Alberts ◽  
Elizabeth A. Archie

In humans and other long-lived species, harsh conditions in early life often lead to profound differences in adult life expectancy. In response, natural selection is expected to accelerate the timing and pace of reproduction in individuals who experience some forms of early-life adversity. However, the adaptive benefits of reproductive acceleration following early adversity remain untested. Here, we test a recent version of this theory, the internal predictive adaptive response (iPAR) model, by assessing whether accelerating reproduction following early-life adversity leads to higher lifetime reproductive success. We do so by leveraging 48 y of continuous, individual-based data from wild female baboons in the Amboseli ecosystem in Kenya, including prospective, longitudinal data on multiple sources of nutritional and psychosocial adversity in early life; reproductive pace; and lifetime reproductive success. We find that while early-life adversity led to dramatically shorter lifespans, individuals who experienced early adversity did not accelerate their reproduction compared with those who did not experience early adversity. Further, while accelerated reproduction predicted increased lifetime reproductive success overall, these benefits were not specific to females who experienced early-life adversity. Instead, females only benefited from reproductive acceleration if they also led long lives. Our results call into question the theory that accelerated reproduction is an adaptive response to both nutritional and psychosocial sources of early-life adversity in baboons and other long-lived species.


2020 ◽  
Author(s):  
Pierre Barry ◽  
Thomas Broquet ◽  
Pierre-Alexandre Gagnaire

AbstractGenetic diversity varies among species due to a range of eco-evolutionary processes that are not fully understood. The neutral theory predicts that the amount of variation in the genome sequence between different individuals of the same species should increase with its effective population size (Ne). In real populations, multiple factors that modulate the variance in reproductive success among individuals cause Ne to differ from the total number of individuals (N). Among these, age-specific mortality and fecundity rates are known to have a direct impact on the ratio. However, the extent to which vital rates account for differences in genetic diversity among species remains unknown. Here, we addressed this question by comparing genome-wide genetic diversity across 16 marine fish species with similar geographic distributions but contrasted lifespan and age-specific survivorship and fecundity curves. We sequenced the whole genome of 300 individuals to high coverage and assessed their genome-wide heterozygosity with a reference-free approach. Individual genome-wide heterozygosity varied from 0.2 to 1.4%, and adult lifespan was by far the most significant predictor of genetic diversity, with a large negative effect (slope = −0.089 per additionnal year of lifespan) that was further increased when brooding species providing intense parental care were removed from the dataset (slope = −0.129 per additionnal year of lifespan). Using published vital rates for each species, we showed that the ratio only generated by life tables predict the observed differences in genetic diversity among species. We further found that the extent of reduction in with increasing adult lifespan is particularly strong under Type III survivorship curves (high juvenile and low adult mortality) and increasing fecundity with age, which is typical of marine fish. Our study highlights the importance of vital rates in the evolution of genetic diversity within species in nature.Author SummaryUnderstanding how and why genetic diversity varies across species has important implications for evolutionary and conservation biology. Although genomics has vastly improved our ability to document intraspecific DNA sequence variation at the genome level, the range and determinants of genetic diversity remain partially understood. At a broad taxonomic scale in eukaryotes, the main determinants of diversity are reproductive strategies distributed along a trade-off between the quantity and the size of offspring, which likely affect the long-term effective population size. Long-lived species also tend to show lower genetic diversity, a result which has however not been reported by comparative studies of genetic diversity at lower taxonomic scales. Here, we compared genetic diversity across 16 European marine fish species showing marked differences in longevity. Adult lifespan was the best predictor of genetic diversity, with genome-wide average heterozygosity ranging from 0.2% in the black anglerfish to 1.4% in the European pilchard. Using life tables summarizing age-specific mortality and fecundity rates for each species, we showed that the variance in lifetime reproductive success resulting from age structure, iteroparity and overlapping generations can predict the range of observed differences in genetic diversity among marine fish species. We then used computer simulations to explore how combinations of vital rates characterizing different life histories affect the relationship between adult lifespan and genetic diversity. We found that marine fishes that display high juvenile but low adult mortality, and increasing fecundity with age, are typically expected to show reduced genetic diversity with increased adult lifespan. However, the impact of adult lifespan vanished using bird and mammal-like vital rates. Our study shows that variance in lifetime reproductive success can have a major impact on a species’ genetic diversity and explains why this effect varies widely across taxonomic groups.


Author(s):  
Logan Luevano ◽  
Chris Sutherland ◽  
Raisa Hernández-Pacheco

Adversity early in life can shape the reproductive potential of individuals through negative effects on health and lifespan. However, long-lived populations with multiple reproductive events may present alternative life history strategies to optimize reproductive schedules and compensate for shorter lifespans when experiencing adversities early in life. Here, we quantify the effects of major hurricanes and density-dependence as sources of early-life ecological adversity on the mean age-specific fertility, reproductive pace, and lifetime reproductive success (LRS) of Cayo Santiago rhesus macaque females, and explored demographic mechanisms for reproductive schedule optimization later in life. Females experiencing major hurricanes early in life exhibit a delayed reproductive debut, but maintain inter-birth intervals and show a higher mean fertility during prime reproductive ages relative to females experiencing no hurricanes. Increasing density at birth is associated to a decrease in mean fertility and LRS. When combined, our study reveals that early-life ecological adversities predict a delay-overshoot pattern in mean age-specific fertility that supports the maintenance of LRS. In contrast to predictive adaptive response models of accelerated reproduction, the long-lived Cayo Santiago population presents a novel reproductive strategy where females who experience major natural disasters early in life ultimately overcome their initial reproductive penalty with no overall negative fitness outcomes. Such strategy suggests that investing more energy into development and maintenance at younger ages allows long-lived females experiencing early-life ecological adversity to reproduce at a mean rate equivalent to that of a typical female cohort later in life.


2021 ◽  
Vol 288 (1951) ◽  
pp. 20210560
Author(s):  
Britt J. Heidinger ◽  
Aurelia C. Kucera ◽  
Jeff D. Kittilson ◽  
David F. Westneat

The mechanisms that contribute to variation in lifetime reproductive success are not well understood. One possibility is that telomeres, conserved DNA sequences at chromosome ends that often shorten with age and stress exposures, may reflect differences in vital processes or influence fitness. Telomere length often predicts longevity, but longevity is only one component of fitness and little is known about how lifetime reproductive success is related to telomere dynamics in wild populations. We examined the relationships between telomere length beginning in early life, telomere loss into adulthood and lifetime reproductive success in free-living house sparrows ( Passer domesticus ). We found that females, but not males, with longer telomeres during early life had higher lifetime reproductive success, owing to associations with longevity and not reproduction per year or attempt. Telomeres decreased with age in both sexes, but telomere loss was not associated with lifetime reproductive success. In this species, telomeres may reflect differences in quality or condition rather than the pace of life, but only in females. Sexually discordant selection on telomeres is expected to influence the stability and maintenance of within population variation in telomere dynamics and suggests that any role telomeres play in mediating life-history trade-offs may be sex specific.


2015 ◽  
Vol 282 (1804) ◽  
pp. 20143053 ◽  
Author(s):  
Adam D. Hayward ◽  
Ilona Nenko ◽  
Virpi Lummaa

The physiology of reproductive senescence in women is well understood, but the drivers of variation in senescence rates are less so. Evolutionary theory predicts that early-life investment in reproduction should be favoured by selection at the cost of reduced survival and faster reproductive senescence. We tested this hypothesis using data collected from preindustrial Finnish church records. Reproductive success increased up to age 25 and was relatively stable until a decline from age 41. Women with higher early-life fecundity (ELF; producing more children before age 25) subsequently had higher mortality risk, but high ELF was not associated with accelerated senescence in annual breeding success. However, women with higher ELF experienced faster senescence in offspring survival. Despite these apparent costs, ELF was under positive selection: individuals with higher ELF had higher lifetime reproductive success. These results are consistent with previous observations in both humans and wild vertebrates that more births and earlier onset of reproduction are associated with reduced survival, and with evolutionary theory predicting trade-offs between early reproduction and later-life survival. The results are particularly significant given recent increases in maternal ages in many societies and the potential consequences for offspring health and fitness.


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