scholarly journals Longer telomeres during early life predict higher lifetime reproductive success in females but not males

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.

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

2021 ◽  
Author(s):  
Michael Le Pepke ◽  
Alina K. Niskanen ◽  
Thomas Kvalnes ◽  
Winnie Boner ◽  
Bernt-Erik Sæther ◽  
...  

ABSTRACTInbreeding can have negative effects on survival and reproduction, which may be of conservation concern in small and isolated populations. However, the physiological mechanisms underlying inbreeding depression are not well-known. The length of telomeres, the DNA sequences protecting chromosome ends, has been associated with health or fitness in several species. We investigated effects of inbreeding on early-life telomere length in two small island populations of wild house sparrows (Passer domesticus) known to be affected by inbreeding depression. Using genomic and pedigree-based measures of inbreeding we found that inbred nestling house sparrows have shorter telomeres. This negative effect of inbreeding on telomere length may have been complemented by a heterosis effect resulting in longer telomeres in individuals that were less inbred than the population average. Furthermore, we found some evidence of stronger effects of inbreeding on telomere length in males than females. Thus, telomere length may reveal subtle costs of inbreeding in the wild and demonstrate a route by which inbreeding negatively impacts the physiological state of an organism already at early life-history stages.


2021 ◽  
Author(s):  
Michael Le Pepke ◽  
Thor Harald Ringsby ◽  
Dan T. A. Eisenberg

Telomeres, the short DNA sequences that protect chromosome ends, are an ancient molecular structure, which is highly conserved across most eukaryotes. Species differ in their telomere lengths, but the causes of this variation are not well understood. Here, we demonstrate that mean early-life telomere length is an evolutionary labile trait across 58 bird species (representing 35 families in 12 orders) with the greatest trait diversity found among passerines. Among these species, telomere length is significantly negatively associated with the fast-slow axis of life-history variation, suggesting that telomere length may have evolved to mediate trade-offs between physiological requirements underlying the diversity of pace-of-life strategies in birds. Curiously, within some species, larger individual chromosome size predicts longer telomere lengths on that chromosome, leading to the suggestion that telomere length also covaries with chromosome length across species. We show that longer mean chromosome length or genome size tends to be associated with longer mean early-life telomere length (measured across all chromosomes) within a phylogenetic framework constituting up to 32 bird species. Combined, our analyses generalize patterns previously found within a few species and provide potential adaptive explanations for the 10-fold variation in telomere lengths observed among birds.


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.


2021 ◽  
Author(s):  
Sophie Bennett ◽  
Antje Girndt ◽  
Alfredo Sánchez-Tójar ◽  
Terry Burke ◽  
Mirre J. P. Simons ◽  
...  

Offspring of older parents in many species display decreased longevity, a faster ageing rate and lower fecundity than offspring born to younger parents. Biomarkers, such as telomeres, that tend to shorten as individual age, may provide insight into the mechanisms of parental age effects. Parental age could determine telomere length either through inheritance of shortened telomeres or through indirect effects, such as variation in parental care with parent ages, which in turn might lead to variation in offspring telomere length. There is no current consensus as to the heritability of telomere length, and the direction and extent of parental age effects however. To address this, here we experimentally investigate how parental age is associated with telomere length at two time points in early life in a captive population of house sparrows (Passer domesticus). We experimentally separated parental age from sex effects by allowing the parent birds to only mate with young, or old partners. We found that telomere length of the offspring increased between the age of 0.5 and 3 months at the group and individual level, which has been reported previously predominantly in non-avian taxa. We further show that older fathers produced daughters with a greater early-life increase in telomere length, supporting sex-specific inheritance, and or sex-specific non-genetic effects. Overall, our results highlight the need for more studies testing early-life telomere dynamics and sex-specific heritability of telomere length.


2020 ◽  
Vol 224 (1) ◽  
pp. jeb231290
Author(s):  
Tiia Kärkkäinen ◽  
Pauliina Teerikorpi ◽  
Wiebke Schuett ◽  
Antoine Stier ◽  
Toni Laaksonen

ABSTRACTEarly-life conditions are crucial determinants of phenotype and fitness. The effects of pre- and post-natal conditions on fitness prospects have been widely studied but their interactive effects have received less attention. In birds, asynchronous hatching creates challenging developmental conditions for the last-hatched chicks, but differential allocation in last-laid eggs might help to compensate this initial handicap. The relative importance and potential interaction between pre- and post-hatching developmental conditions for different fitness components remains mostly unknown. We manipulated hatching order in wild pied flycatchers (Ficedula hypoleuca), creating three groups: natural asynchrony (last-laid eggs hatching last), reversed asynchrony (last-laid eggs hatching first) and hatching synchrony (all eggs hatching at once). We examined the effects of these manipulations on early-life survival, growth and telomere length, a potential cellular biomarker of fitness prospects. Mortality was mostly affected by hatching order, with last-hatched chicks being more likely to die. Early-life telomere dynamics and growth were influenced by the interplays between laying and hatching order. Last-laid but first-hatched chicks were heavier but had shorter telomeres 5 days after hatching than their siblings, indicating rapid early growth with potential adverse consequences on telomere length. Synchronous chicks did not suffer any apparent cost of hatching synchronously. Impaired phenotypes only occurred when reversing the natural hatching order (i.e. developmental mismatch), suggesting that maternal investment in last-laid eggs might indeed counterbalance the initial handicap of last-hatched chicks. Our experimental study thus highlights that potential interplays between pre- and post-natal environments are likely to shape fitness prospects in the wild.


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):  
Michael Le Pepke ◽  
Thomas Kvalnes ◽  
Peter Sjolte Ranke ◽  
Yimen G. Araya-Ajoy ◽  
Jonathan Wright ◽  
...  

1.Environmental conditions during early-life development can have lasting effects on individual quality and fitness. Telomere length (TL) may correlate with early-life conditions and may be an important mediator or biomarker of individual quality or pace-of-life, as periods of increased energy demands can increase telomere attrition due to oxidative stress. Thus, knowledge of the mechanisms that generate variation in TL, and the relation between TL and fitness, is important in understanding the role of telomeres in ecology and life-history evolution. 2.Here, we investigate how environmental conditions and morphological traits are associated with early-life TL and if TL predicts natal dispersal probability or components of fitness in two populations of wild house sparrows (Passer domesticus). 3.We measured morphological traits and blood TL in 2746 nestlings from 20 cohorts (1994-2013) and retrieved data on weather conditions. We monitored population fluctuations, and individual survival and reproductive output using field observations and genetic pedigrees. We then used generalized linear mixed-effects models to test which factors affected TL in early-life, and if TL predicted dispersal propensity, or was associated with recruitment probability, mortality risk, or reproductive success.4.We found a negative effect of population density on TL, but only in one of the populations. There was a curvilinear association between TL and the maximum daily North Atlantic Oscillation (NAO) index during incubation, suggesting that there are optimal weather conditions that result in the longest TL. Dispersers tended to have shorter telomeres than non-dispersers. TL did not predict survival, but we found a tendency for individuals with short telomeres to have higher annual reproductive success.5.Our study showed how early-life TL is shaped by effects of growth, weather conditions and population density, supporting that environmental stressors negatively affect TL in wild populations. In addition, TL may be a mediator or biomarker of individual pace-of-life, with higher dispersal rates and annual reproduction tending to be associated with shorter early-life TL in this study. However, clear associations between early-life TL and individual fitness seems difficult to establish and may differ between different populations in the wild.


Author(s):  
Michael Pepke ◽  
Thomas Kvalnes ◽  
Bernt Rønning ◽  
Henrik Jensen ◽  
Winnie Boner ◽  
...  

Changes in telomere dynamics could underlie life-history trade-offs among growth, size and longevity, but our ability to quantify such mechanistic processes in natural, unmanipulated populations is limited. We investigated how 4 years of artificial selection for either larger or smaller body size affected early-life telomere length in two insular populations of wild house sparrows. A negative correlation between telomere length and structural size was evident under both selection regimes. The study also revealed that male sparrows had longer telomeres than females, after controlling for size, and there was a significant negative effect of harsh weather conditions on telomere length. The long-term fitness consequences of these changes in early-life telomere length induced by the artificial size selection were explored over a period of 11 years. These analyses indicated disruptive selection on telomere length because both short and long early-life telomere length tended to be associated with the lowest mortality rates and highest life expectancy. There was also weak evidence for a negative association between telomere length and annual reproductive success, but only in the population where body size was increased experimentally. Our results suggest that natural selection for optimal body size in wild animals will affect early-life telomere length during growth, which is known to be linked to longevity in birds, but also that the importance of telomeres for long-term somatic maintenance and fitness is complex in a wild bird species.


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