Intergenerational Transfer of Ageing: Parental Age and Offspring Lifespan
Authors: Pat Monaghan, Alexei A. Maklakov, Neil B. Metcalfe
Journal: Trends in Ecology & Evolution (2020)

The quality and viability of offspring depends on the age at which the parents breed.A reduced lifespan in offspring from older parents is known as the Lansing effect.It is found across many taxa but does not always occur.The many mechanisms that can produce this effect is highlighted.The Lansing effect does not necessarily imply a reduction in offspring fitness. 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. 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. Understanding how and why ageing occurs, what factors determine its rate, and why this varies among species and individuals, is a topic of intense research by scientists from diverse disciplines [1.Wolf N.S. The Comparative Biology of Aging. Springer, 2010Crossref Scopus (6) Google Scholar, 2.López-Otín C. et al.The hallmarks of aging.Cell. 2013; 153: 1194-1217Abstract Full Text Full Text PDF PubMed Scopus (7742) Google Scholar, 3.Shefferson R.P. The Evolution of Senescence in the Tree of Life. Cambridge University Press, 2017Crossref Scopus (40) Google Scholar]. However, almost all of the focus has been on the time-dependent, somatic deterioration of individuals during their lifetimes. Studies of the relationship between age and reproductive performance have primarily been concerned with effects on parent rather than offspring fitness [4.Lemaître J.F. Gaillard J.M. Reproductive senescence: new perspectives in the wild.Biol. Rev. 2017; 92: 2182-2199Crossref PubMed Scopus (105) Google Scholar]. However, the age of parents can potentially have a multitude of effects on offspring phenotypes, both positive and negative, and not necessarily involving parental ageing [4.Lemaître J.F. Gaillard J.M. Reproductive senescence: new perspectives in the wild.Biol. Rev. 2017; 92: 2182-2199Crossref PubMed Scopus (105) Google Scholar]. Here we focus on the widely reported negative effect of the age of parents at a breeding event (hereafter termed 'parental age') on offspring lifespan, which has become known as the Lansing effect. Knowing whether, and under what conditions, parental age can have a negative effect on offspring lifespan has profound implications for our understanding of the evolution of animal life histories, and for more applied fields such as reproductive medicine and conservation biology. In many iteroparous species, the relationship between the age of parents and their reproductive output is a bell-shaped curve (Box 1), but it has been known for a surprisingly long time that parental age can affect the lifespan of offspring as well as their number. In 1918 Alexander Graham Bell (inventor of the telephone) conducted pioneering demographic analyses based on the extensive family tree of an early American settler. He found that offspring of the youngest parents lived a decade longer than those of the oldest [5.Bell A.G. The duration of life and conditions associated with longevity - a study of the Hyde geneology. Geneological Record Office, 1918Google Scholar]. Subsequent experimental studies by Jennings and Lynch working with parthenogenic rotifers, found a similar negative relationship between parental age at the time of reproduction and offspring lifespan [6.Jennings H.S. Lynch R.S. Age, mortality, fertility, and individual diversities in the rotifer Proales sordida Gosse I Effect of age of the parent on characteristics of the offspring.J. Exp. Zool. 1928; 50: 345-407Crossref Scopus (24) Google Scholar]. In 1947, Albert Lansing further showed that rotifer selection lines in which the parents were old breeders had shorter-lived offspring and died out much sooner than lines in which the parents were consistently young breeders [7.Lansing A.I. A transmissible, cumulative, and reversible factor in aging.J. Gerontol. 1947; 2: 228-239Crossref PubMed Scopus (123) Google Scholar]. Based on these results, Lansing envisioned a 'transmissible and cumulative ageing factor', more of which was transmitted to offspring of older parents and which could thereby accumulate across the generations.Box 1The Changing Relationship between Parental Age and Reproductive OutputA bell-shaped relationship (Figure I) between parental age and breeding performance has been found in many iteroparous species, both in the laboratory and in studies of wild populations [4.Lemaître J.F. Gaillard J.M. Reproductive senescence: new perspectives in the wild.Biol. Rev. 2017; 92: 2182-2199Crossref PubMed Scopus (105) Google Scholar,63.Forslund P. Pärt T. Age and reproduction in birds - hypotheses and tests.Trends Ecol. Evol. 1995; 10: 374-378Abstract Full Text PDF PubMed Scopus (639) Google Scholar,64.Monaghan P. et al.The evolutionary ecology of senescence.Funct. Ecol. 2008; 22: 371-378Crossref Scopus (236) Google Scholar]. At a population level, this pattern can be generated by the selective disappearance of low-quality individuals at a young age, and a longer lifespan of individuals with lower investment per breeding attempt; a relationship between the age of first breeding and reproductive performance can also contribute, for example, if poor performing individuals tend to breed at a younger age. However, similar bell shaped patterns are also found within individual animals, as a result of gaining resources, experience and/or status in their early years, and then in later life having impaired breeding performance due to the effects of ageing [4.Lemaître J.F. Gaillard J.M. Reproductive senescence: new perspectives in the wild.Biol. Rev. 2017; 92: 2182-2199Crossref PubMed Scopus (105) Google Scholar]. While the same bell-shaped pattern can be evident in a range of reproductive traits, such as egg size or egg quality [65.Benton T.G. et al.Maternal effects mediated by maternal age: from life histories to population dynamics.J. Anim. Ecol. 2008; 77: 1038-1046Crossref PubMed Scopus (91) Google Scholar], most ecological-based studies have focussed on demographic parameters, most usually offspring number (taken as a measure of the reproductive success of the parents), with less attention being paid to offspring quality or fate [13.Barks P.M. Laird R.A. Senescence in duckweed: age-related declines in survival, reproduction and offspring quality.Funct. Ecol. 2015; 29: 540-548Crossref Scopus (33) Google Scholar]. Studies aiming to investigate whether a Lansing effect occurs need to be designed carefully to take account of the likely initial improvement in offspring quality with parental age; the comparison should not involve young breeders (Figure I, part A of curve), but instead should be a comparison between middle-aged and old breeders B versus C. Comparison at A and C, or A and B could erroneously suggest no effect, or a positive effect. A bell-shaped relationship (Figure I) between parental age and breeding performance has been found in many iteroparous species, both in the laboratory and in studies of wild populations [4.Lemaître J.F. Gaillard J.M. Reproductive senescence: new perspectives in the wild.Biol. Rev. 2017; 92: 2182-2199Crossref PubMed Scopus (105) Google Scholar,63.Forslund P. Pärt T. Age and reproduction in birds - hypotheses and tests.Trends Ecol. Evol. 1995; 10: 374-378Abstract Full Text PDF PubMed Scopus (639) Google Scholar,64.Monaghan P. et al.The evolutionary ecology of senescence.Funct. Ecol. 2008; 22: 371-378Crossref Scopus (236) Google Scholar]. At a population level, this pattern can be generated by the selective disappearance of low-quality individuals at a young age, and a longer lifespan of individuals with lower investment per breeding attempt; a relationship between the age of first breeding and reproductive performance can also contribute, for example, if poor performing individuals tend to breed at a younger age. However, similar bell shaped patterns are also found within individual animals, as a result of gaining resources, experience and/or status in their early years, and then in later life having impaired breeding performance due to the effects of ageing [4.Lemaître J.F. Gaillard J.M. Reproductive senescence: new perspectives in the wild.Biol. Rev. 2017; 92: 2182-2199Crossref PubMed Scopus (105) Google Scholar]. While the same bell-shaped pattern can be evident in a range of reproductive traits, such as egg size or egg quality [65.Benton T.G. et al.Maternal effects mediated by maternal age: from life histories to population dynamics.J. Anim. Ecol. 2008; 77: 1038-1046Crossref PubMed Scopus (91) Google Scholar], most ecological-based studies have focussed on demographic parameters, most usually offspring number (taken as a measure of the reproductive success of the parents), with less attention being paid to offspring quality or fate [13.Barks P.M. Laird R.A. Senescence in duckweed: age-related declines in survival, reproduction and offspring quality.Funct. Ecol. 2015; 29: 540-548Crossref Scopus (33) Google Scholar]. Studies aiming to investigate whether a Lansing effect occurs need to be designed carefully to take account of the likely initial improvement in offspring quality with parental age; the comparison should not involve young breeders (Figure I, part A of curve), but instead should be a comparison between middle-aged and old breeders B versus C. Comparison at A and C, or A and B could erroneously suggest no effect, or a positive effect. Early studies that followed Lansing were primarily concerned with the potential cumulative effect over successive generations, with several failing to reproduce it [8.Lints F.A. Hoste C. Lansing effect revisited 1. Life-span.Exp. Gerontol. 1974; 9: 51-69Crossref PubMed Scopus (46) Google Scholar,9.Lints F.A. Hoste C. Lansing effect revisited 2. Cumulative and spontaneously reversible parental age effects on fecundity in Drosophila melanogaster.Evolution. 1977; 31: 387-404Crossref PubMed Google Scholar]. More recently, lifespan has mostly only been studied in the first (F1) generation of offspring (for exceptions see [10.Plaistow S.J. et al.Offspring provisioning explains clone-specific maternal age effects on life history and life span in the water flea, Daphnia pulex.Am. Nat. 2015; 186: 376-389Crossref PubMed Scopus (35) Google Scholar, 11.Qazi M.C.B. et al.Transgenerational effects of maternal and grandmaternal age on offspring viability and performance in Drosophila melanogaster.J. Insect Physiol. 2017; 100: 43-52Crossref PubMed Scopus (19) Google Scholar, 12.Wylde Z. et al.Parental breeding age effects on descendants' longevity interact over 2 generations in matrilines and patrilines.PLoS Biol. 2019; 17e3000556Crossref PubMed Scopus (19) Google Scholar]), and the phenomenon of older parents giving rise to shorter-lived offspring has become known as the Lansing effect irrespective of any intergenerational accumulation. However, the existence of the Lansing effect has largely been ignored by theories on the evolution of ageing and life histories, which usually assume that the fitness of offspring is independent of parental age at conception [13.Barks P.M. Laird R.A. Senescence in duckweed: age-related declines in survival, reproduction and offspring quality.Funct. Ecol. 2015; 29: 540-548Crossref Scopus (33) Google Scholar]. There are exceptions (e.g., see [14.McNamara J.M. et al.Deterioration, death and the evolution of reproductive restraint in late life.Proc. R. Soc. B. 2009; 276: 4061-4066Crossref PubMed Scopus (112) Google Scholar, 15.Moorad J.A. Nussey D.H. Evolution of maternal effect senescence.Proc. Natl. Acad. Sci. U. S. A. 2016; 113: 362-367Crossref PubMed Scopus (43) Google Scholar, 16.Barks P.M. Laird R.A. Parental age effects and the evolution of senescence.Am. Nat. 2020; 195: 886-898Crossref PubMed Scopus (13) Google Scholar,77.Hernández C.M. et al.A demographic and evolutionary analysis of maternal effect senescence.Proc. Nat. Acad. Sci. U. S. A. 2020; 117: 16431-16437Crossref PubMed Scopus (11) Google Scholar]), but even a model that explicitly examines the link between parental age and offspring life expectancy [17.van den Heuvel J. et al.Disposable soma theory and the evolution of maternal effects on ageing.PLoS ONE. 2016; 11e0145544Crossref PubMed Scopus (18) Google Scholar] excludes the possibility that gametes can age, and so underplays the potential for the Lansing effect. The need for gametic ageing to be included has recently emphasised [18.Galipaud M. Kokko H. Sex, senescence, sources and sinks.Funct. Ecol. 2020; 34: 55-64Crossref Scopus (6) Google Scholar,19.Galipaud M. Kokko H. Adaptation and plasticity in life-history theory: how to derive predictions.Evol. Hum. Behav. 2020; (Published online June 19, 2020. https://doi.org/10.1016/j.evolhumbehav.2020.06.007)Crossref Scopus (13) Google Scholar] since it is important that we understand the selection pressures that shape optimal reproductive scheduling and thereby the pattern of parental investment that organisms show across their lifetimes, which would be strongly influenced by intergenerational transfer of ageing if this impacts offspring fitness [16.Barks P.M. Laird R.A. Parental age effects and the evolution of senescence.Am. Nat. 2020; 195: 886-898Crossref PubMed Scopus (13) Google Scholar]. It is also important to distinguish between the two quite distinct processes that can separately or together generate a shorter lifespan, namely an increased 'frailty', manifested as an increased mortality rate at any time of life, and an increased rate of ageing, which only becomes apparent later in life (Figure 1). We also need to understand the mechanisms underlying any Lansing effect, since this will help explain whether the Lansing effect arises as a result of constraints (e.g., somatic or germline deterioration) or adaptations (e.g., changes in reproductive scheduling). The Lansing effect is defined here as an empirically demonstrated negative relationship between parental age and offspring lifespan, irrespective of whether this is due to an increase in offspring ageing rate or frailty. Discussed later, is the need to consider the Lansing effect as part of a broader framework encompassing parental age effects on offspring fitness. Table 1 gives examples of studies that have found offspring early survival or average lifespan to be negatively related to the age of the parent(s); further examples are given in [10.Plaistow S.J. et al.Offspring provisioning explains clone-specific maternal age effects on life history and life span in the water flea, Daphnia pulex.Am. Nat. 2015; 186: 376-389Crossref PubMed Scopus (35) Google Scholar,12.Wylde Z. et al.Parental breeding age effects on descendants' longevity interact over 2 generations in matrilines and patrilines.PLoS Biol. 2019; 17e3000556Crossref PubMed Scopus (19) Google Scholar]. The table serves to illustrate the taxonomic breadth of the organisms in which Lansing effects have been found, that they occur in both field and laboratory studies, and that few have determined whether the shorter lifespan is due to increased offspring frailty, more rapid ageing or both. It is important to emphasise that not all reported effects of parental age on offspring viability or lifespan are negative, and reported effects are sometimes inconsistent. For example, different studies of Drosophila have found the effect of increasing parental age on offspring survival or lifespan to be negative [20.Price D.K. Hansen T.F. How does offspring quality change with age in male Drosophila melanogaster?.Behav. 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Stud. 2012; 51: 72-84Google Scholar], neutral [25.Yilmaz M. et al.Maternal age effects on longevity in Drosophila melanogaster populations of different origin.Biogerontology. 2008; 9: 163-168Crossref PubMed Scopus (10) Google Scholar], or strain-specific [26.Lee J.H. et al.Strain-specific effects of parental age on offspring in Drosophila melanogaster.Entomol. Res. 2019; 49: 187-202Crossref Scopus (4) Google Scholar]. Some of this inconsistency could be due to aspects of study design: Table 1 emphasises that most studies to date have used a cross-sectional study design, which can lead to problems in data interpretation (Box 1). Older parents may produce longer-lived offspring if they have increased access to resources and/or greater experience, or engage in increased reproductive effort if their life expectancy is short ('terminal investment') [27.Poizat G. et al.Empirical evidence of a trade-off between reproductive effort and expectation of future reproduction in female three-spined sticklebacks.Proc. R. Soc. Lond. B. 1999; 266: 1543-1548Crossref Scopus (55) Google Scholar,28.Boonekamp J.J. et al.Experimentally increased brood size accelerates actuarial senescence and increases subsequent reproductive effort in a wild bird population.J. Anim. Ecol. 2020; 89: 1395-1407Crossref PubMed Scopus (12) Google Scholar]. It is also the case that conspecifics will age at different rates, and that this will affect the pattern of intergenerational transfer.Table 1Examples of the Lansing Effect (Where Offspring of Older Parents Have Shorter Lifespans), Chosen to Demonstrate the Breadth of Affected Taxa and Range of ApproachesTaxon and referenceField or labExperimental or natural pairingsaWhether parents were assigned mates by the researcher or formed their own natural pairings.Virgin parents?bWhether both young and old parents were virgins at time of producing the offspring whose survival was measured.Paternal effect on lifespancBrackets indicate either that it is not known whether both sexes contribute to the effect, or that the species is asexual.Maternal effect on lifespancBrackets indicate either that it is not known whether both sexes contribute to the effect, or that the species is asexual.Nature of Lansing effectEffects within individuals?dWhether the analyses showed a Lansing effect within individual animals, (e.g., by using within-subject centring) [76]. Note that the majority of studies adopt a cross-sectional approach so cannot test for changes with age within individuals.Nematode Heligmosomoides polygyrus [69.Lippens C. et al.Aging parasites produce offspring with poor fitness prospects.Biol. Lett. 2017; 13: 20160888Crossref PubMed Scopus (11) Google Scholar]LabNaturalNo(Yes)(Yes)Reduced larval-adult survival in offspring of older worms (not known whether both parents contribute to effect)NoRotifer Brachionus manjavacas [70.Bock M.J. et al.Maternal age alters offspring lifespan, fitness, and lifespan extension under caloric restriction.Sci. Rep. 2019; 9: 3138Crossref PubMed Scopus (24) Google Scholar]Lab–No(Yes) - asexualHigher initial mortality rate and lower median lifespan in offspring of older mothers, but slower rate of ageingNoWater flea Daphnia pulex [10.Plaistow S.J. et al.Offspring provisioning explains clone-specific maternal age effects on life history and life span in the water flea, Daphnia pulex.Am. Nat. 2015; 186: 376-389Crossref PubMed Scopus (35) Google Scholar]Lab–NoYesShorter lifespan and faster rate of ageing in two of the three clonesNoFruit fly Drosophila melanogaster [23.Priest N.K. et al.The role of parental age effects on the evolution of aging.Evolution. 2002; 56: 927-935Crossref PubMed Scopus (152) Google Scholar]LabExperimentalYesNoYesShorter lifespan of daughters of older mothers in most strains; due to an increase in frailty rather than rate of ageingNoButterfly Pieris brassicae [71.Ducatez S. et al.Complex interactions between paternal and maternal effects: parental experience and age at reproduction affect fecundity and offspring performance in a butterfly.Evolution. 2012; 66: 3558-3569Crossref PubMed Scopus (49) Google Scholar]LabExperimentalNoYesShorter lifespan in offspring of older mothersNoRice weevil Sitophilus oryzae [72.Opit G.P. Throne J.E. Influence of maternal age on the fitness of progeny in the rice weevil, Sitophilus oryzae (Coleoptera: Curculionidae).Environ. Entomol. 2007; 36: 83-89Crossref PubMed Scopus (22) Google Scholar]LabExperimentalNoYesShorter lifespan in offspring of older mothersNoCommon tern Sterna hirundo [57.Bouwhuis S. et al.Sex-specific pathways of parental age effects on offspring lifetime reproductive success in a long-lived seabird.Evolution. 2015; 69: 1760-1771Crossref PubMed Scopus (53) Google Scholar]FieldNaturalNoYesNoShorter lifespan in sons of older fathers; no effects in other combinationsNoWandering albatross Diomedea exulans [58.Fay R. et al.Paternal but not maternal age influences early-life performance of offspring in a long-lived seabird.Proc. R. Soc. B. 2016; 283: 20152318Crossref PubMed Scopus (34) Google Scholar]FieldNaturalNoYesNoLower juvenile survival in offspring of older fathers; no effects of mother's ageYesHoubara bustard Chlamydotisundulata [55.Vuarin P. et al.Post-copulatory sexual selection allows females to alleviate the fitness costs incurred when mating with senescing males.Proc. R. Soc. B. 2019; 286: 20191675Crossref PubMed Scopus (13) Google Scholar]Lab then fieldExperimentalNoYesLower juvenile survival in daughters of older fathers (no effect in sons)NoMouse Mus musculus [54.Tarín J.J. et al.Delayed motherhood decreases life expectancy of mouse offspring.Biol. Reprod. 2005; 72: 1336-1343Crossref PubMed Scopus (36) Google Scholar]LabExperimentalYesYesShorter lifespan in offspring of older femalesNoRed squirrel Tamiasciurus hudsonicus [73.Descamps S. et al.Age-specific variation in survival, reproductive success and offspring quality in red squirrels: evidence of senescence.Oikos. 2008; 117: 1406-1416Crossref Scopus (84) Google Scholar]FieldNaturalNoYesLower juvenile post-weaning survival (to 1 year) of offspring of older femalesNoAsian elephant Elephas maximus [74.Reichert S. et al.Maternal age at birth shapes offspring life-history trajectory across generations in long-lived Asian elephants.J. Anim. Ecol. 2020; 89: 996-1007Crossref PubMed Scopus (15) Google Scholar]FieldNaturalNoYesLower survival in offspring of older mothers and older grandmothersNoHuman Homo sapiens [75.Gillespie D.O.S. et al.The effect of maternal age and reproductive history on offspring survival and lifetime reproduction in preindustrial humans.Evolution. 2013; 67: 1964-1974Crossref PubMed Scopus (46) Google Scholar]FieldNaturalNoYesLower survival to adulthood in offspring of older mothersYesa Whether parents were assigned mates by the researcher or formed their own natural pairings.b Whether both young and old parents were virgins at time of producing the offspring whose survival was measured.c Brackets indicate either that it is not known whether both sexes contribute to the effect, or that the species is asexual.d Whether the analyses showed a Lansing effect within individual animals, (e.g., by using within-subject centring) [76.van de Pol M.V. Wright J. A simple method for distinguishing within- versus between-subject effects using mixed models.Anim. Behav. 2009; 77: 753-758Crossref Scopus (645) Google Scholar]. Note that the majority of studies adopt a cross-sectional approach so cannot test for changes with age within individuals. Open table in a new tab Nonexclusive routes whereby the age of parents could affect the lifespan of their offspring are described herein. It is important to remember that the Lansing effect can arise via routes that have nothing to do with ageing of the parents or their offspring, as described in Box 2. It should be also noted that most of these potential mechanisms relate more to the biological rather than the chronological age of the parents, and may be influenced by, for instance, prior reproductive effort or environmental harshness, both of which influence rates of ageing [4.Lemaître J.F. Gaillard J.M. Reproductive senescence: new perspectives in the wild.Biol. Rev. 2017; 92: 2182-2199Crossref PubMed Scopus (105) Google Scholar,29.Nussey D.H. et al.Senescence in natural populations of animals: widespread evidence and its implications for bio-gerontology.Ageing Res. Rev. 2013; 12: 214-225Crossref PubMed Scopus (430) Google Scholar]. However, in practice it tends to be the chronological age that is measured. A distinction is drawn here between direct effects of the age-related deterioration of the parents or their germ cells on offspring, and indirect effects of parental age such as changes in investment patterns by mates, or compensatory responses by the offspring themselves. Unless otherwise stated, the mechanisms discussed below could operate through either parent.Box 2Mechanisms That Can Generate Apparent Lansing Effects Even When There Is No Age-Related Change in ParentsProcesses at both the tissue and population level can give the spurious impression of reproductive senescence within individuals reducing the viability of offspring. Firstly, consider the way in which a female's oocytes are used across her breeding lifespan. In species such as birds and mammals the full complement of a female's germ cells appears to be present at sexual maturity. If these vary in quality, then it would be adaptive to use the best oocytes first, and only use poorer oocytes later in life since the chances of living to breed in old age may be low [66.Duran H.E. et al.The association of reproductive senescence with mitochondrial quantity, function, and DNA integrity in human oocytes at different stages of maturation.Fertil. Steril. 2011; 96: 384-388Abstract Full Text Full Text PDF PubMed Scopus (84) Google Scholar]. This effect can arise if the last oocytes to be used have been through more cell divisions and have more genetic damage or reduced telomere length, as would appear to be the case, for example, in long-lived mammals [67.Polani P.E. Crolla J.A. A test of the production line hypothesis of mammalian oogenesis.Hum. Genet. 1991; 88: 64-70Crossref PubMed Scopus (79) Google Scholar]. Under this scenario, offspring quality would decline with maternal age even if there was no change over time in the state of each oocyte (or of the mother) (Figure IA). An alternative process operates in population level studies, where analyses can show a lower mean lifespan in the offspring produced by older parents, without any decline in the lifespan of offspring produced by individual parents. This can arise if there is a link between the level of investment in offspring per breeding event, and the probability of parents surviving into old age, as has been found for example, in wild red-billed choughs Pyrrhocorax phyrrhocorax [68.Reid J.M. et al.Parent age, lifespan and offspring survival: structured variation in life history in a wild population.J. Anim. Ecol. 2010; 79: 851-862PubMed Google Scholar]. Thus individual 1 in Figure IB invests heavily in each offspring but over a short reproductive lifespan, while individual 2 invests less per offspring but has a longer reproductive lifespan (and so produces more offspring) as a consequence. These two scenarios represent extremes of a continuum of alternative reproductive strategies that may have similar lifetime fitness. However, taking the population as a whole, there is then a decrease in the lifespan of offspring as mean parental age increases, because the only offspring being produced by older parents are those that receive less investment, and so are less viable [68.Reid J.M. et al.Parent age, lifespan and offspring survival: structured variation in life history in a wild population.J. Anim. Ecol. 2010; 79: 851-862PubMed Google Scholar]. Processes at both the tissue and population level can give the spurious impression of reproductive senescence within individuals reducing the viability of offspring. Firstly, consider the way in which a female's oocytes are used across her breeding lifespan. In species such as birds and mammals the full complement of a female's germ cells appears to be present at sexual maturity. If these var