Maternal and Paternal Age Effects on Male Antler Flies: A Field Experiment.

AbstractIn many species, parental age at reproduction can influence offspring performance and life span, but the direction of these effects and the traits affected vary among studies. Data on parental age effects are still scarce in noncaptive 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 life span and reproductive success of their male offspring released in the wild. Increased paternal, but not maternal, age somewhat increased sons' adult life span, 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.

Inverse Lansing Effect: Maternal Age and Provisioning Affecting Daughters' Longevity and Male Offspring Production.

AbstractMaternal age effects on offspring life history are known in a variety of organisms, with offspring of older mothers typically having lower life expectancy (the Lansing effect). However, there is no consensus on the generality and mechanisms of this pattern. We tested predictions of the Lansing effect in several Daphnia magna clones and observed clone-specific magnitude and direction of the maternal age effect on offspring longevity. We also report ambidirectional, genotype-specific effects of maternal age on the propensity of daughters to produce male offspring. Focusing on two clones with contrasting life histories, we demonstrate that maternal age effects can be explained by lipid provisioning of embryos by mothers of different ages. Individuals from a single-generation maternal age reversal treatment showed intermediate life span and intermediate lipid content at birth. In the clone characterized by the "inverse Lansing effect," neonates produced by older mothers showed higher mitochondrial membrane potential in neural tissues than their counterparts born to younger mothers. We conclude that an inverse Lansing effect is possible and hypothesize that it may be caused by age-specific maternal lipid provisioning creating a calorically restricted environment during embryonic development, which in turn reduces fecundity and increases life span in offspring.

Cross-Generational Effects of Parental Age on Offspring Longevity: Are Telomeres an Important Underlying Mechanism?

Parental age at offspring conception often influences offspring longevity, but the mechanisms underlying this link are poorly understood. One mechanism that may be important is telomeres, highly conserved, repetitive sections of non-coding DNA that form protective caps at chromosome ends and are often positively associated with longevity. Here, the potential pathways by which the age of the parents at the time of conception may impact offspring telomeres are described first, including direct effects on parental gamete telomeres and indirect effects on offspring telomere loss during pre- or post-natal development. Then a surge of recent studies demonstrating the effects of parental age on offspring telomeres in diverse taxa are reviewed. In doing so, important areas for future research and experimental approaches that will enhance the understanding of how and when these effects likely occur are highlighted. It is concluded by considering the potential evolutionary consequences of parental age on offspring telomeres.

Beneficial cumulative effects of old parental age on offspring fitness.

Old parental age is commonly associated with negative effects on offspring life-history traits. Such parental senescence effects are predicted to have a cumulative detrimental effect over successive generations. However, old parents may benefit from producing higher quality offspring when these compete for seasonal resources. Thus, old parents may choose to increase investment in their offspring, thereby producing fewer but larger and more competitive progeny. We show that Caenorhabditis elegans hermaphrodites increase parental investment with advancing age, resulting in fitter offspring who reach their reproductive peak earlier. Remarkably, these effects increased over six successive generations of breeding from old parents and were subsequently reversed following a single generation of breeding from a young parent. Our findings support the hypothesis that offspring of old parents receive more resources and convert them into increasingly faster life histories. These results contradict the theory that old parents transfer a cumulative detrimental 'ageing factor' to their offspring.

The deteriorating soma and the indispensable germline: gamete senescence and offspring fitness.

The idea that there is an impenetrable barrier that separates the germline and soma has shaped much thinking in evolutionary biology and in many other disciplines. However, recent research has revealed that the so-called 'Weismann Barrier' is leaky, and that information is transferred from soma to germline. Moreover, the germline itself is now known to age, and to be influenced by an age-related deterioration of the soma that houses and protects it. This could reduce the likelihood of successful reproduction by old individuals, but also lead to long-term deleterious consequences for any offspring that they do produce (including a shortened lifespan). Here, we review the evidence from a diverse and multidisciplinary literature for senescence in the germline and its consequences; we also examine the underlying mechanisms responsible, emphasizing changes in mutation rate, telomere loss, and impaired mitochondrial function in gametes. We consider the effect on life-history evolution, particularly reproductive scheduling and mate choice. Throughout, we draw attention to unresolved issues, new questions to consider, and areas where more research is needed. We also highlight the need for a more comparative approach that would reveal the diversity of processes that organisms have evolved to slow or halt age-related germline deterioration.

Intergenerational effects on offspring telomere length: interactions among maternal age, stress exposure and offspring sex.

Offspring produced by older parents often have reduced longevity, termed the Lansing effect. Because adults usually have similar-aged mates, it is difficult to separate effects of maternal and paternal age, and environmental circumstances are also likely to influence offspring outcomes. The mechanisms underlying the Lansing effect are poorly understood. Variation in telomere length and loss, particularly in early life, is linked to longevity in many vertebrates, and therefore changes in offspring telomere dynamics could be very important in this context. We examined the effect of maternal age and environment on offspring telomere length in zebra finches. We kept mothers under either control (ad libitum food) or more challenging (unpredictable food) circumstances and experimentally minimized paternal age and mate choice effects. Irrespective of the maternal environment, there was a substantial negative effect of maternal age on offspring telomere length, evident in longitudinal and cross-sectional comparisons (average of 39% shorter). Furthermore, in young mothers, sons reared by challenged mothers had significantly shorter telomere lengths than sons reared by control mothers. This effect disappeared when the mothers were old, and was absent in daughters. These findings highlight the importance of telomere dynamics as inter-generational mediators of the evolutionary processes determining optimal age-specific reproductive effort and sex allocation.

Experimental demonstration that offspring fathered by old males have shorter telomeres and reduced lifespans.

Offspring of older parents frequently show reduced longevity, but the mechanisms driving this so-called 'Lansing effect' are unknown. While inheritance of short telomeres from older parents could underlie this effect, studies to date in different species have found mixed results, reporting positive, negative or no association between parental age and offspring telomere length (TL). However, most of the existing evidence is from non-experimental studies in which it is difficult to exclude alternative explanations such as differential survival of parents with different telomere lengths. Here we provide evidence in the zebra finch that offspring from older parents have reduced lifespans. As a first step in disentangling possible causes, we used an experimental approach to examine whether or not we could detect pre-natal paternal effects on offspring TL. We found that zebra finch embryos fathered by old males have shorter telomeres than those produced by the same mothers but with younger fathers. Since variation in embryonic TL persists into post-natal life, and early life TL is predictive of longevity in this species, this experimental study demonstrates that a paternally driven pre-natal TL reduction could at least in part underlie the reduced lifespan of offspring from older parents.

Reduced telomere length in offspring of old fathers in a long-lived seabird.

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.

A multigenerational effect of parental age on offspring size but not fitness in common duckweed (Lemna minor).

Classic theories on the evolution of senescence make the simplifying assumption that all offspring are of equal quality, so that demographic senescence only manifests through declining rates of survival or fecundity. However, there is now evidence that, in addition to declining rates of survival and fecundity, many organisms are subject to age-related declines in the quality of offspring produced (i.e. parental age effects). Recent modelling approaches allow for the incorporation of parental age effects into classic demographic analyses, assuming that such effects are limited to a single generation. Does this 'single-generation' assumption hold? To find out, we conducted a laboratory study with the aquatic plant Lemna minor, a species for which parental age effects have been demonstrated previously. We compared the size and fitness of 423 laboratory-cultured plants (asexually derived ramets) representing various birth orders, and ancestral 'birth-order genealogies'. We found that offspring size and fitness both declined with increasing 'immediate' birth order (i.e. birth order with respect to the immediate parent), but only offspring size was affected by ancestral birth order. Thus, the assumption that parental age effects on offspring fitness are limited to a single generation does in fact hold for L. minor. This result will guide theorists aiming to refine and generalize modelling approaches that incorporate parental age effects into evolutionary theory on senescence.

Maternal age effects on offspring lifespan and reproduction vary within a species.

Across diverse taxa, offspring from older mothers have decreased lifespan and fitness. Little is known about the extent to which maternal age effects vary among genotypes for a given species, however, except for studies of a few arthropod species. To investigate the presence and degree of intraspecific variability in maternal age effects, we compared lifespan, reproductive schedule, and lifetime reproductive output of offspring produced by young, middle-aged, and old mothers in four strains of rotifers in the Brachionus plicatilis species complex. We found significant variability among strains in the magnitude and direction of maternal age effects on offspring life history traits. In one strain, offspring of young mothers lived 20% longer than offspring of old mothers, whereas there were no significant effects of maternal age on lifespan for other strains. Depending on strain, advanced maternal age had positive effects, negative effects, or no effect on lifetime reproductive output. Across strains, older mothers produced offspring that had higher maximum daily reproduction early in life. The effects of maternal age on offspring vital rates could not be explained by changes in trade-offs between lifespan and reproduction. This study documents intraspecific variability in maternal age effects in an additional clade. Investigating intraspecific variability is critical for understanding the ubiquity of maternal age effects and their role in the evolution of life history and aging.

What does not kill you makes you stronger? Effects of paternal age at conception on fathers and sons.

Advancing male age is often hypothesized to reduce both male fertility and offspring quality due to reproductive senescence. However, the effects of advancing male age on reproductive output and offspring quality are not always deleterious. For example, older fathers might buffer the effects of reproductive senescence by terminally investing in reproduction. Similarly, males that survive to reproduce at an old age might carry alleles that confer high viability (viability selection), which are then inherited by offspring, or might have high reproductive potential (selective disappearance). Differentiating these mechanisms requires an integrated experimental study of paternal survival and reproductive performance, as well as offspring quality, which is currently lacking. Using a cross-sectional study in Drosophila melanogaster, we test the effects of paternal age at conception (PAC) on paternal survival and reproductive success, and on the lifespans of sons. We discover that mating at an old age is linked with decreased future male survival, suggesting that mating-induced mortality is possibly due to old fathers being frail. We find no evidence for terminal investment and show that reproductive senescence in fathers does not onset until their late-adult life. Additionally, we find that as a father's lifespan increases, his probability of siring offspring increases for older PAC treatments only. Lastly, we show that sons born to older fathers live longer than those born to younger fathers due to viability selection. Collectively, our results suggest that advancing paternal age is not necessarily associated with deleterious effects for offspring and may even lead to older fathers producing longer-lived offspring.

Evidence of Paternal Effects on Telomere Length Increases in Early Life.

Offspring of older parents in many species have decreased longevity, a faster ageing rate and lower fecundity than offspring born to younger parents. Biomarkers of ageing, such as telomeres, that tend to shorten as individuals age, may provide insight into the mechanisms of such parental age effects. Parental age may be associated with offspring telomere length either directly through inheritance of shortened telomeres or indirectly, for example, through changes in parental care in older parents affecting offspring telomere length. Across the literature there is considerable variation in estimates of the heritability of telomere length, and in the direction and extent of parental age effects on telomere length. To address this, we experimentally tested how parental age is associated with the early-life telomere dynamics of chicks at two time points in a captive population of house sparrows Passer domesticus. We experimentally separated parental age from sex effects, and removed effects of age-assortative mating, by allowing the parent birds to only mate with young, or old partners. The effect of parental age was dependent on the sex of the parent and the chicks, and was found in the father-daughter relationship only; older fathers produced daughters with longer telomere lengths post-fledging. Overall we found that chick telomere length increased between the age of 0.5 and 3 months at the population and individual level. This finding is unusual in birds with such increases more commonly associated with non-avian taxa. Our results suggest parental age effects on telomere length are sex-specific either through indirect or direct inheritance. The study of similar patterns in different species and taxa will help us further understand variation in telomere length and its evolution.

Heritability and Parental Effects in Telomere Length in a Color Polymorphic Long-Lived Bird.

AbstractRelative telomere length (RTL), an indicator of senescence, has been shown to be heritable but can also be affected by environmental factors, such as parental effects. Investigating heritability as well as parental effects and rearing environment can help us to understand the factors affecting offspring telomeres. Moreover, how phenotypic parental traits linked with fitness can impact offspring RTL is still unclear. A phenotypic marker closely associated with physiological traits and fitness is melanin-based color polymorphism, which in tawny owl (Strix aluco) is highly heritable and strongly associated with adult telomere shortening and survival. We studied narrow-sense heritability (h2) of RTL, as well as the impact of parental age and color morph and their interaction on offspring RTL. Offspring RTL at fledging was strongly positively correlated with both mother RTL and father RTL at breeding. Offspring RTL was also negatively associated with father age, suggesting that older fathers sired offspring with shorter telomeres. Parental color morph did not explain offspring RTL, and there were no interactive effects of parental morph and age, despite previously documented morph-specific senescence patterns. Our results suggest that RTL is highly heritable and affected by paternal age but not related to color polymorphism. This suggests that either morph-specific telomere shortening as an adult does not result in significantly shorter telomeres in their gametes, or that parents compensate morph-specific senescence via parental care. Morph-specific patterns of telomere dynamics in polymorphic species may thus emerge from different life history strategies adopted in adulthood.

Sex-dependent effects of parental age on offspring fitness in a cooperatively breeding bird.

Parental age can have considerable effects on offspring phenotypes and health. However, intergenerational effects may also have longer term effects on offspring fitness. Few studies have investigated parental age effects on offspring fitness in natural populations while also testing for sex- and environment-specific effects. Further, longitudinal parental age effects may be masked by population-level processes such as the selective disappearance of poor-quality individuals. Here, we used multigenerational data collected on individually marked Seychelles warblers (Acrocephalus sechellensis) to investigate the impact of maternal and paternal age on offspring life span and lifetime reproductive success. We found negative effects of maternal age on female offspring life span and lifetime reproductive success, which were driven by within-mother effects. There was no difference in annual reproductive output of females born to older versus younger mothers, suggesting that the differences in offspring lifetime reproductive success were driven by effects on offspring life span. In contrast, there was no association between paternal age and female offspring life span or either maternal or paternal age and male offspring life span. Lifetime reproductive success, but not annual reproductive success, of male offspring increased with maternal age, but this was driven by between-mother effects. No paternal age effects were found on female offspring lifetime reproductive success but there was a positive between-father effect on male offspring lifetime reproductive success. We did not find strong evidence for environment-dependent parental age effects. Our study provides evidence for parental age effects on the lifetime fitness of offspring and shows that such effects can be sex dependent. These results add to the growing literature indicating the importance of intergenerational effects on long-term offspring performance and highlight that these effects can be an important driver of variation in longevity and fitness in the wild.

Intergenerational Transfer of Ageing: Parental Age and Offspring Lifespan.

The extent to which the age of parents at reproduction can affect offspring lifespan and other fitness-related traits is important in our understanding of the selective forces shaping life history evolution. In this article, the widely reported negative effects of parental age on offspring lifespan (the 'Lansing effect') is examined. Outlined herein are the potential routes whereby a Lansing effect can occur, whether effects might accumulate across multiple generations, and how the Lansing effect should be viewed as part of a broader framework, considering how parental age affects offspring fitness. The robustness of the evidence for a Lansing effect produced so far, potential confounding variables, and how the underlying mechanisms might best be unravelled through carefully designed experimental studies are discussed.

Sex-specific pathways of parental age effects on offspring lifetime reproductive success in a long-lived seabird.

The conditions under which individuals are reared vary and sensitivity of offspring to such variation is often sex-dependent. Parental age is one important natal condition with consequences for aspects of offspring fitness, but reports are mostly limited to short-term fitness consequences and do not take into account offspring sex. Here we used individual-based data from a large colony of a long-lived seabird, the common tern Sterna hirundo, to investigate longitudinal long-term fitness consequences of parental age in relation to both offspring and parental sex. We found that recruited daughters from older mothers suffered from reduced annual reproductive success. Recruited sons from older fathers were found to suffer from reduced life span. Both effects translated to reductions in offspring lifetime reproductive success. Besides revealing novel sex-specific pathways of transgenerational parental age effects on offspring fitness, which inspire studies of potential underlying mechanisms, our analyses show that reproductive senescence is only observed in the common tern when including transgenerational age effects. In general, our study shows that estimates of selective pressures underlying the evolution of senescence, as well as processes such as age-dependent mate choice and sex allocation, will depend on whether causal transgenerational effects exist and are taken into account.