scholarly journals Telomere heritability and parental age at conception effects in a wild avian population

2020 ◽  
Author(s):  
Alexandra Sparks ◽  
Lewis G. Spurgin ◽  
Marco van der Velde ◽  
Eleanor A. Fairfield ◽  
Jan Komdeur ◽  
...  

Individual variation in telomere length is predictive of health and mortality risk across a range of species. However, the relative influence of environmental and genetic variation on individual telomere length in wild populations remains poorly understood. In previous studies, heritability of telomere length has primarily been calculated using parent-offspring regression, but shared environments can confound such estimates. Furthermore, associations with age and parental age at conception effects are typically not accounted for but can also bias heritability estimates. To control for these confounding variables, quantitative genetic ‘animal models’ can be used. However, the few studies on wild populations using this approach have been restricted by power. Here, we investigated the heritability of telomere length and parental age at conception effects in the Seychelles warbler using 2664 telomere length measures from 1318 birds over 20 years and a multi-generational pedigree. We found a weak negative within-paternal age at conception effect (as fathers aged, their offspring had shorter telomeres) and a weak positive between-maternal age at conception effect (females that survived to older ages had offspring with longer telomeres). While parent–offspring regressions did not detect heritability, animal models provided evidence that heritability of telomere length was low in this population. Environmental and technical variation largely influenced telomere length and would have biased heritability estimates if unaccounted for. Estimating the heritability of telomere length is complex, requiring large sample sizes and accounting for confounding effects in order to improve our understanding of the evolutionary potential of telomere length in the wild.

2005 ◽  
Vol 272 (1571) ◽  
pp. 1415-1425 ◽  
Author(s):  
Anne Charmantier ◽  
Dany Garant

An essential requirement to determine a population's potential for evolutionary change is to quantify the amount of genetic variability expressed for traits under selection. Early investigations in laboratory conditions showed that the magnitude of the genetic and environmental components of phenotypic variation can change with environmental conditions. However, there is no consensus as to how the expression of genetic variation is sensitive to different environmental conditions. Recently, the study of quantitative genetics in the wild has been revitalized by new pedigree analyses based on restricted maximum likelihood, resulting in a number of studies investigating these questions in wild populations. Experimental manipulation of environmental quality in the wild, as well as the use of naturally occurring favourable or stressful environments, has broadened the treatment of different taxa and traits. Here, we conduct a meta-analysis on recent studies comparing heritability in favourable versus unfavourable conditions in non-domestic and non-laboratory animals. The results provide evidence for increased heritability in more favourable conditions, significantly so for morphometric traits but not for traits more closely related to fitness. We discuss how these results are explained by underlying changes in variance components, and how they represent a major step in our understanding of evolutionary processes in wild populations. We also show how these trends contrast with the prevailing view resulting mainly from laboratory experiments on Drosophila . Finally, we underline the importance of taking into account the environmental variation in models predicting quantitative trait evolution.


2018 ◽  
Author(s):  
Christina Bauch ◽  
Jelle J. Boonekamp ◽  
Peter Korsten ◽  
Ellis Mulder ◽  
Simon Verhulst

AbstractTelomere length (TL) predicts health and lifespan in humans and other organisms, making the identification of the causes of TL variation of interest. At conception, zygotes inherit genes that regulate TL during early development, but at the same time already express a phenotype, which is the TL of the parental gametes that formed the zygote. Whether the effect of gamete TL is transient or affects TL for life depends on the extent to which regulatory genes compensate for gamete TL variation during early development. A carry-over effect of parental TL, resulting in epigenetic inheritance, has been suggested to explain the observed relationship between parental age and offspring TL in humans and other species. However, reports of parental age effects are based on cross-sectional data, and age at reproduction has numerous confounds. Furthermore, parental age may affect offspring telomere dynamics between conception and sampling, which could also explain the paternal age effect. Using longitudinal telomere data of jackdaw parents and their chicks, we show that chicks hatched with shorter telomeres as individual fathers aged, whereas mother age had no effect. By cross-fostering eggs, we confirmed the paternal age effect to be independent of paternal care after conception. The epigenetic effect accounted for 34% of the variance in offspring TL that was explained by paternal telomere length; the remaining 66% we ascribe to a combination of environmental and additive genetic effects. Thus, our results strongly indicate epigenetic inheritance of TL, with potential consequences for offspring fitness prospects.Significance statementTelomeres are DNA-protein structures at chromosome ends and their length predicts remaining lifespan in humans and other organisms. Variation in telomere length is thought to be largely of genetic origin, but telomere inheritance may be unusual because a fertilised cell already has a telomere length (most traits are first expressed later in life). Telomeres shorten with age, and, using long-term individual-based data of jackdaw families, we show that as fathers aged, they produced chicks with shorter telomeres. This shows that paternal telomere length directly affects offspring telomere length, i.e. is inherited genetically but without the involvement of genes. This is known as an epigenetic effect and explained a large part (≥34%) of the telomere resemblance between fathers and their offspring.


2018 ◽  
Author(s):  
L Gervais ◽  
C Perrier ◽  
M Bernard ◽  
J Merlet ◽  
J Pemberton ◽  
...  

AbstractEstimating the evolutionary potential of quantitative traits and reliably predicting responses to selection in wild populations are important challenges in evolutionary biology. The genomic revolution has opened up opportunities for measuring relatedness among individuals with precision, enabling pedigree-free estimation of trait heritabilities in wild populations. However, until now, most quantitative genetic studies based on a genomic relatedness matrix (GRM) have focused on long-term monitored populations for which traditional pedigrees were also available, and have often had access to knowledge of genome sequence and variability. Here, we investigated the potential of RAD-sequencing for estimating heritability in a free-ranging roe deer population for which no prior genomic resources were available. We propose a step-by-step analytical framework to optimize the quality and quantity of the genomic data and explore the impact of the SNP calling and filtering processes on the GRM structure and GRM-based heritability estimates. As expected, our results show that sequence coverage strongly affects the number of recovered loci, the genotyping error rate and the amount of missing data. Ultimately, this had little effect on heritability estimates and their standard errors, provided that the GRM was built from a minimum number of loci (above 7000). GRM-based heritability estimates thus appear robust to a moderate level of genotyping errors in the SNP dataset. We also showed that quality filters, such as the removal of low-frequency variants, affect the relatedness structure of the GRM, generating lower h2 estimates. Our work illustrates the huge potential of RAD-sequencing for estimating GRM-based heritability in virtually any natural population.


2018 ◽  
Vol 14 (6) ◽  
pp. 20180213 ◽  
Author(s):  
Sandra Bouwhuis ◽  
Simon Verhulst ◽  
Christina Bauch ◽  
Oscar Vedder

Evidence for transgenerational effects of senescence, whereby offspring from older parents have a reduced lifetime reproductive success, is increasing. Such effects could arise from compromised germline maintenance in old parents, potentially reflected in reduced telomere length in their offspring. We test the relationship between parental age and offspring early-life telomere length in a natural population of common terns and find a significant negative correlation between paternal age and offspring telomere length. Offspring telomere length is reduced by 35 base pairs for each additional year of paternal age. We find no correlation with maternal age. These results fit with the idea of compromised germline maintenance in males, whose germline stem cells require continued division.


2021 ◽  
Author(s):  
Christopher Angell ◽  
Rebecca Janacek ◽  
Howard D Rundle

In many species, parental age at reproduction can influence offspring performance and lifespan, but the direction of these effects and the traits affected vary among studies. Data on parental age effects are still scarce in non-captive populations, especially insects, despite species such as fruit flies being models in laboratory-based aging research. We performed a biologically relevant experimental manipulation of maternal and paternal age at reproduction of antler flies (Protopiophila litigata) in the laboratory and tracked the adult lifespan and reproductive success of their male offspring released in the wild. Increased paternal, but not maternal, age somewhat increased sons’ adult lifespan, while parental ages did not influence sons’ mating rate or reproductive senescence. Our results indicate that while parental age effects do exist in an insect in the field, they may be beneficial in such a short-lived animal, in contrast to results from most wild vertebrates and laboratory invertebrates.


2021 ◽  
Vol 40 (3) ◽  
pp. 211-217
Author(s):  
Brayden Whitlock

Arsenic is both a chemotherapeutic drug and an environmental toxicant that affects hundreds of millions of people each year. Arsenic exposure in drinking water has been called the worst poisoning in human history. How arsenic is handled in the body is frequently studied using rodent models to investigate how arsenic both causes and treats disease. These models, used in a variety of arsenic-related testing, from tumor formation to drug toxicity monitoring, have virtually always been developed from animals with telomeres that are unnaturally long, likely because of accidental artificial selective pressures. Mice that have been bred in captivity in laboratory conditions, often for over 100 years, are the standard in creating animal models for this research. Using these mice introduces challenges to any work that can be affected by the length of telomeres and the related capacities for tissue repair and cancer resistance. However, arsenic research is particularly susceptible to the misuse of such animal models due to the multiple and various interactions between arsenic and telomeres. Researchers in the field commonly find mouse models and humans behaving very differently upon exposure to acute and chronic arsenic, including drug therapies which seem safe in mice but are toxic in humans. Here, some complexities and apparent contradictions of the arsenic carcinogenicity and toxicity research are reconciled by an explanatory model that involves telomere length explained by the evolutionary pressures in laboratory mice. A low-risk hypothesis is proposed which has the power to determine whether researchers can easily develop more powerful and accurate mouse models by simply avoiding mouse lineages that are very old and have strangely long telomeres. Swapping in newer mouse lineages for the older, long-telomere mice may vastly improve our ability to research arsenic toxicity with virtually no increase in cost or difficulty of research.


2013 ◽  
Vol 59 (4) ◽  
pp. 485-505 ◽  
Author(s):  
Jon E. Brommer

Abstract Individual-based studies allow quantification of phenotypic plasticity in behavioural, life-history and other labile traits. The study of phenotypic plasticity in the wild can shed new light on the ultimate objectives (1) whether plasticity itself can evolve or is constrained by its genetic architecture, and (2) whether plasticity is associated to other traits, including fitness (selection). I describe the main statistical approach for how repeated records of individuals and a description of the environment (E) allow quantification of variation in plasticity across individuals (IxE) and genotypes (GxE) in wild populations. Based on a literature review of life-history and behavioural studies on plasticity in the wild, I discuss the present state of the two objectives listed above. Few studies have quantified GxE of labile traits in wild populations, and it is likely that power to detect statistically significant GxE is lacking. Apart from the issue of whether it is heritable, plasticity tends to correlate with average trait expression (not fully supported by the few genetic estimates available) and may thus be evolutionary constrained in this way. Individual-specific estimates of plasticity tend to be related to other traits of the individual (including fitness), but these analyses may be anti-conservative because they predominantly concern stats-on-stats. Despite the increased interest in plasticity in wild populations, the putative lack of power to detect GxE in such populations hinders achieving general insights. I discuss possible steps to invigorate the field by moving away from simply testing for presence of GxE to analyses that ‘scale up’ to population level processes and by the development of new behavioural theory to identify quantitative genetic parameters which can be estimated.


2021 ◽  
Author(s):  
Tomos Potter ◽  
Anja Felmy

AbstractIn wild populations, large individuals have disproportionately higher reproductive output than smaller individuals. We suggest an ecological explanation for this observation: asymmetry within populations in rates of resource assimilation, where greater assimilation causes both increased reproduction and body size. We assessed how the relationship between size and reproduction differs between wild and lab-reared Trinidadian guppies. We show that (i) reproduction increased disproportionately with body size in the wild but not in the lab, where effects of resource competition were eliminated; (ii) in the wild, the scaling exponent was greatest during the wet season, when resource competition is strongest; and (iii) detection of hyperallometric scaling of reproduction is inevitable if individual differences in assimilation are ignored. We propose that variation among individuals in assimilation – caused by size-dependent resource competition, niche expansion, and chance – can explain patterns of hyperallometric scaling of reproduction in natural populations.


2020 ◽  
Author(s):  
Bincai Wei ◽  
Yantao Shao ◽  
Jun Liang ◽  
Peng Tang ◽  
Meile Mo ◽  
...  

Abstract Background: Telomere length (TL) is variable at birth and is inversely associated with body mass index (BMI) in adulthood. A growing number of evidences suggested that a higher maternal pre-pregnancy BMI results in adverse offspring health outcomes, especially shorter newborn TL. However, a newborn’s genetic endowment is equally derived from both parents, the association between parental pre-pregnancy BMI and newborn TL has been rarely discussed. We aimed to determine the association between parental pre-pregnancy BMI and newborn TL. Methods: A total of 1082 parent-newborn pairs were recruited from the Guangxi Zhuang Birth Cohort (GZBC). TL in cord blood was measured using quantitative real-time polymerase chain reaction (qPCR) and expressed as the ratio of telomere copy number to single-copy gene number (T/S). A series of linear regressions were performed to assess the associations between parental pre-pregnancy BMI and newborn TL.Results: Mothers who were overweight before pregnancy had significantly shorter cord blood telomere length in their newborns than those who were normal weight before pregnancy [percentage change: −8.17% (95% CI: −14.69 to −0.92%; P=0.028)]. Further analysis of the combined effects of parental weight status on newborn TL showed that TL was significantly shortened among newborns whose mothers were overweight and fathers were of healthy weight when compared with those whose mothers and fathers were both of normal weight [percentage change: −8.59% (95% CI: −15.47 to −1.14%; P=0.025)]. Subgroup analysis indicated these effects were more pronounced among male newborns and those whose paternal age <31 years or maternal age ≥28 years at delivery. Conclusions: Maternal pre-pregnancy overweight, but not paternal pre-pregnancy overweight is associated with shorter newborn TL. Weight control in reproductive women and effective eugenics intervention programs may be of particular benefit for improving longevity and life quality of offspring.


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.


Sign in / Sign up

Export Citation Format

Share Document