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Life-history theory, reproduction and longevity in humans

Abstract and Keywords

The basic assumption underlying life-history theory is that natural selection has selected for an optimal combination of life-history traits that maximizes individual fitness. The best studied trade-offs include: investigating how individuals should allocate resources to reproduction versus their own growth and survival; and when reproducing, how should they divide their effort between current and future reproduction or between the number, sex, and quality of offspring. Co-ordinated evolution of all these principal life-history traits together determines the life-history strategy of the organism. The environment, in turn, determines the action of natural selection: traits may be adaptive only within reference to a particular environment and few, if any, traits are adaptive in all contexts. Life-history theory proposes that, generally, there should be no selection for living beyond one's reproductive capacity. Instead, the ‘surplus’ energy reserves which would allow post-reproductive survival are predicted to be better off spent earlier in one's life, during reproductive years.

Keywords: life-history theory, natural selection, fitness, reproduction, growth, survival, sex, offspring, environment

27.1. Introduction

27.1.1. Life-history theory

Our success, in evolutionary terms, can be measured by the total number of children we produce in our lifetimes which survive to pass our genes on to the following generations. The lifetime reproductive success of individuals depends on two main factors: their reproductive ability and their survival. However, because resources available to individuals are finite and the two body functions, reproduction and self-maintenance, compete for the same pool of energy, increasing the flow of resources to one body function (e.g. reproduction) will necessarily reduce the flow of resources to others (e.g. growth, body condition and maintenance of effective immune defence). This can result in a negative relationship (trade-off) between the two functions, which will constrain an individual's ability to maximize all fitness-related life-history traits at the same time. It is for this reason that increased reproductive effort is predicted to shorten lifespan, and individuals must find the best compromise between these two different components (and others) to be able to maximize their lifetime reproductive success.

The theoretical framework within which we study how individuals optimize trade-offs in life-history traits is called ‘life-history theory’. This refers to the scheduling of major events over the lifetime of individuals. For example, how big should one be at the moment of birth? How fast and how long should one grow? At what age and size should maturation take place? How many offspring should be produced, and when, what size and of which sex? How long should one continue reproducing, and when is it time to die? Different solutions to these evolutionary problems ultimately determine an individual's representation in the future generations (i.e. fitness). The basic assumption underlying life-history theory is that natural selection has selected for an optimal combination of life-history traits that maximizes individual fitness (Lessells, 1991; Roff, 1992, 2002; Stearns, 1992). The best studied trade-offs include: (i) investigating how individuals should allocate resources to reproduction versus their own growth and survival; and (ii) when reproducing, how should they divide their effort between current and future reproduction or between the number, sex and quality of offspring (Lack, 1954; Gadgil and Bossert, 1970; Schaffer, 1974, (p. 398) Charlesworth and Leon, 1976; Charlesworth, 1980; Williams, 1966a, b). Co-ordinated evolution of all these principal life-history traits together determines the life-history strategy of the organism (Stearns, 1976). The environment, in turn, determines the action of natural selection: traits may be adaptive only within reference to a particular environment and few, if any, traits are adaptive in all contexts.

27.1.2. The human life-history trade-offs

All of these trade-offs would be predicted to be pertinent to humans (Hill and Kaplan, 1999). In addition, however, humans have an extra trade-off, that is absent or uncommon in other animals. Life-history theory proposes that, generally, there should be no selection for living beyond one's reproductive capacity. Instead, the ‘surplus’ energy reserves which would allow post-reproductive survival are predicted to be better off spent earlier in one's life, during reproductive years (Williams, 1957; Hamilton, 1966). In addition, relative levels of investment during reproductive attempts should influence the age at which individuals senesce and die (Kirkwood, 1977; Partridge and Harvey, 1985; Kirkwood and Rose, 1991; Kirkwood and Austad, 2000). In line with this, age-related reductions in fertility rates have been observed in long-lived animals (Ricklefs et al., 2003), and virtually all animals reproduce until they die (or have very short post-reproductive lifespans; Cohen, 2004). However, there is at least one striking exception: women commonly survive long after losing the ability to reproduce themselves (Williams, 1957; Hamilton, 1966), and evidence suggests that this prolonged survival is related to humans allocating more resources to cell maintenance and repair than other animals (Hawkes, 2003). This prolonged lifespan is not an artefact of modern society. The age at which humans terminate reproduction is consistent with the age of termination in other primates when differences in body weight are accounted for (Schultz, 1969). In addition, in both historical and traditional hunter-gatherer populations, about 30% of adult individuals are beyond the age of 45 years (Hawkes, 2004). This large proportion of old, non-reproductive women in human populations also marks a fundamental difference with other primates. In chimpanzees (Pan troglodytes), female fertility declines at the same age as in humans to virtually zero by age 45 years (Nishida et al., 2003), but chimpanzee survival rates, as predicted by life-history theory, follow fertility rates so that less than 3% of adults are over 45 years old (Hill et al., 2001). That women begin a physiological shut-down of reproductive potential around the age of 45 (Peccei, 2001b) but often continue to survive for another 25 years is enigmatic from an evolutionary point of view. Only in short-finned pilot whales (Globicephala macrorhyncus) and a few other species of cetaceans is there also good evidence of a menopause and significantly prolonged post-reproductive life-span (Marsh and Kasuzya, 1984; McAuliffe and Whitelead, 2005).

Importantly, prolonged post-reproductive survival is associated with fitness benefits in human women. Post-reproductive women gain fitness both by increasing the survival and/or reproductive capacity of their own offspring (Lahdenperä et al, 2004; Tymicki, 2004) as well as the survival of their grand-offspring (Hawkes et al., 1997, 1998; Sear et al., 2000; Jamison et al., 2002; Voland and Beise, 2002; Hawkes, 2003; Lahdenperä et al., 2004; Gibson and Mace, 2005; Voland et al., 2005). Whatever the evolutionary origin of this enigmatic life-history trait, that women accrue fitness during both reproductive and post-reproductive phases means that the reproductive success gained prior to menopause represents only a proportion of total fitness in humans. This has fascinating implications regarding optimal fitness-maximizing tactics, rates of senescence and lifespan in humans.

In most animals, individual fitness is maximized by optimizing the trade-off between current and future reproduction, with the amount of selection on early reproduction relative to late reproduction influencing, in part, the rate at which individuals senesce and die. However, research on humans has shown that increasing current reproductive effort may not only reduce future reproductive success (Mace and Sear, 1997; Lummaa, 2001) but also post-reproductive survival rates, for example due to increased susceptibility to infectious disease (Helle et al., 2002, 2004). This suggests that for humans, high investment in a current attempt not only has a negative effect on an individual's ability to invest in future reproductive attempts but also on the (p. 399) ability to help with the reproductive attempts of offspring following menopause. Consequently, fitness in humans is governed by optimization of trade-offs both within the reproductive and between the reproductive and post-reproductive phases. This leads to the intriguing possibility that humans suffer from both reproductive and post-reproductive senescence, with the relative importance of fitness accrued during each phase influencing ultimate lifespan. However, how natural selection ultimately affects the evolution of life-history traits within these trade-offs depends not only on the fitness benefits and costs of variation in such traits, but also on the genetic architecture of the traits, i.e. the amount of heritable, additive genetic variance present in each life history trait and the genetic correlations between them (Kruuk et al., 2000).

The aim of this chapter is threefold. I will illustrate: (i) how increasing reproductive effort has been found to affect future reproductive success and longevity in humans; (ii) what the benefits of long lifespan are, and given the trade-off between current and future reproductive success and survival, how long should one aim to live in order to maximize long-term fitness in the population; and (iii) how this trade-off between reproduction and survival can constrain how natural selection will affect the evolution of both reproductive effort and longevity in humans. In other words, is there significant heritable variation in the life-history traits, senescence rate and fitness, and how do genetic correlations between these traits influence the evolution of life history? I consider all of these trade-offs for the fitness of women only, for measuring reproductive effort in men is difficult and paternity uncertainty often constrains one from making coherent generalizations.

27.2. Trade-offs between current reproduction and future success

27.2.1 Current reproductive effort and future reproduction

It is clear that individual offspring benefit from having greater parental investment directed at them. Offspring from wealthy parents in general have better health, survival and marital prospects than those born in less privileged backgrounds (Borgerhoff Mulder, 2000). Short inter-birth intervals have negative consequences for the offspring whose parental investment was cut short by the birth of the younger sibling (Blurton Jones, 1986). Babies born with higher birth weight have higher survival probability and can also have superior health and increased reproductive success in adulthood (reviewed in Lummaa and Clutton-Brock, 2002; Lummaa, 2003). However, because high investment in current offspring is predicted to reduce the resources available for both investment in future offspring and self-maintenance, an iteroparous (having >1 reproductive event/lifetime) mother must trade-off current with future reproductive investment to maximize her lifetime reproductive success (Stearns, 1992; Kaplan, 1996; Hill and Kaplan, 1999). Current investment varies with brood/litter size and, if costs of producing males and females differ, the sex ratio of those offspring (reviewed in Charnov, 1982; Clutton-Brock, 1991). In sexually size-dimorphic species, the number and gender of offspring in a current litter are therefore predicted to modify future reproductive investment decisions as well as reproductive success and survival.

Studies on sexually size-dimorphic mammals provide support for the prediction that litters of different sizes and sex ratios can entail differential costs to the mother. In red deer (Cervus elaphus), those females that successfully raised a calf the previous season had the lowest survival, fecundity and body condition next year compared to those mothers that either did not reproduce or lost their offspring soon after birth (Clutton-Brock et al., 1989). In addition, females commonly show longer birth intervals (Lee and Moss, 1986; Boesch, 1997; Cameron and Linklater, 2000) and reduced subsequent litter sizes (Clark et al., 1990) after producing offspring of the more expensive gender. For example, in red deer where male calves are born larger, mothers that previously reared a male calf were more likely to die the following winter and, if they survived, less likely to produce a calf the following season compared to mothers that reared females (Clutton-Brock et al., 1983).

Humans are modestly sexually size-dimorphic and, although singletons are typically delivered, 0.6–4.5% of all births (depending on the population) are twins. Twins are usually born smaller (p. 400) than singletons (Bulmer, 1970). In addition, females (twin and singleton) have slower intrauterine growth rates (Marsál et al., 1996) and lighter birth weights (Hoffman et al., 1974; Loos et al., 2001) than males (twin or singleton). Mortality and morbidity following birth are usually male-biased, and foetal growth of males is more retarded than that of females under stressful conditions (reviewed in Stinson, 1985; Wells, 2000). Moreover, giving birth to a son even in modern-day conditions is significantly more laborious than giving birth to a daughter (Eogan et al., 2003). There is also some evidence that maternal energy intake per day is elevated if a mother is carrying a male foetus (Tamimi et al., 2003), and that mothers in good physiological condition might be more likely to give birth to sons than daughters (Cagnacci et al., 2003, 2004; Gibson and Mace, 2003; but see Stein et al., 2003a, b). This evidence indicates that producing a son is physiologically more demanding to the mother than producing a daughter. Hence, the costs of producing offspring appear to be gender-specific in humans and males tend to be the more expensive gender to produce.

There is mixed evidence to suggest that reproductive history in different modern human societies may affect measures of maternal physiological condition (e.g. stature, weight or body mass index; reviewed in Tracer, 2002). Nevertheless, studies on humans living in a range of settings have shown that increased reproductive effort during a given reproductive attempt may reduce later reproductive success. First, in a study on pre-industrial rural Finns, women doubling the number of children produced in a single reproductive event, by giving birth to twins, were more likely to fail to raise their next offspring, or to completely terminate reproduction, as compared with mothers producing a singleton child at the same age and with the same previous birth history (Lummaa, 2001). Moreover, women that did successfully raise offspring after a twin delivery were more likely next to produce a less expensive female offspring as compared with after an unsuccessful twin delivery, and this effect was further influenced by the sex ratio of the twins produced. This is in line with findings showing that the energetic costs of lactation to the mother may be almost twice as high as those of gestation (Prentice and Whitehead, 1987; Dufour and Sauther, 2002), stressing the importance of including also the survivorship of offspring into the calculations of costs of reproduction. Second, it took a longer time for Gabbra pastoralist mothers who had previously produced a male child to reproduce again, compared to mothers producing a daughter (Mace and Sear, 1997). Finally, in contemporary British mothers, the birth weight of the second-born child was lower if the previous child was a son rather than a daughter (I. J. Rickard, unpublished results).

Taken together, these studies suggest that an increase in the current reproductive effort (producing twins or offspring of the more expensive gender) requires greater maternal investment and can have greater detrimental effects on maternal reproduction in the future. It still remains to be examined whether the gender and survival of the previous offspring affects the subsequent child's reproductive success, but such effects are found in populations of wild mammals (Clutton-Brock, 1991). That such long-term consequences of maternal investment for offspring reproductive success are feasible in humans (reviewed in Lummaa and Clutton-Brock, 2002; Lummaa, 2003) was shown in a study on pregnant women experiencing the Dutch Hunger Winter at the end of Second World War (1944–1945). Female babies exposed to famine in utero themselves had offspring of lower birth weight that suffered from higher mortality before and after birth, compared to mothers not exposed to famine as a foetus (Lumey, 1992).

27.2.2. Current reproductive effort and future survival

Increasing current reproductive effort is not only predicted to reduce future reproductive success, but also the future survival rate of mothers. Theories of senescence based on evolutionary trade-offs highlight the adverse effects of high and early reproductive effort on late-life survival (Williams 1957; Kirkwood, 1977; Kirkwood and Rose, 1991). These predictions are upheld in a variety of animals (e.g. Partridge and Barton, 1993; Kirkwood and Austad, 2000; Partridge and Gems, 2002), although they (p. 401) are often difficult to show in nature (Clutton-Brock, 1991).

As discussed in this volume (Mace, Chapter 26 and Voland, Chapter 28), life-history trade-offs are generally difficult to study adequately using natural variation in reproductive output and parental survival because differences in reproductive output may often reflect adaptive tactics made by individuals of different quality (‘phenotypic correlations’; Daan and Tinbergen, 1997). For example, women with low resource levels may adaptively adjust their family size or reduce investment in each child, to meet their energetic needs and reduce the costs of reproduction (Sear et al., 2003). Perhaps not surprisingly then, evidence for reproduction-mediated decreases in longevity in humans is at best unequivocal. In historical human populations, only few studies have been able to establish the expected negative effects of high total reproductive effort on post-reproductive longevity (Westendorp and Kirkwood, 1998; Thomas et al., 2000; Doblhammer and Oeppen, 2003; Smith et al., 2003). While there is also some evidence that this trade-off is manifest only among the poorest individuals (Kumle and Lund, 2000; Lycett et al., 2000), most studies find no association between total number of children produced and post-reproductive survival, and some even show a positive correlation between these two traits (Borgerhoff Mulder, 1988; Voland and Engel, 1989; Le Bourg et al., 1993; Wrigley et al., 1997; Korpelainen, 2000, 2003; Müller et al., 2002).

Given the obvious limitations of studies on human life-histories due to an inability to experimentally manipulate family size or reproductive effort, alternative ways of investigating effects of effort on subsequent survivorship need to be used. Moreover, these alternative methods clearly need to be able to control adequately for correlates of maternal quality. One method is to use multivariate statistics that control for differences in maternal condition, resource availability, and environmental conditions, although data that would allow such analyses are relatively rare. Another method is to investigate the effects of increasing reproductive effort in a given reproductive attempt on mortality risk in the same mothers using multivariate statistics with random terms. In the following paragraphs, I will discuss the evidence for tradeoffs between investment and mortality risk by comparing mortality rates of mothers after doubling the number of offspring produced in a reproductive attempt (twins) and producing offspring of the more expensive gender (sons). Of particular note is that significant effects of high investment on maternal mortality appear more detectable when analyses consider high reproductive effort in terms of the production of twins or sons rather than the production of a large family size per se. This is an important point, for most of the studies that have failed to find a negative association between maternal investment and survival have not only failed to consider maternal quality but have considered reproductive investment in terms of family size only.

27.2.2.1. Effects of twinning on maternal survival

Producing twins essentially requires a woman to double her reproductive effort in a given reproductive event. Consequently, twins require mothers to allocate twice as much energy to reproduction and less to somatic maintenance according to the disposable soma theory (Kirkwood and Rose, 1991). It is known that mothers who deliver singletons in quick succession may suffer from maternal depletion syndrome; an inability to restore nutritional reserves after childbirth and breastfeeding (Dewey, 1997). That twin deliveries pose an elevated cost to mothers (particularly if they survive to weaning) is supported by the findings that, after twin births, mothers have longer birth intervals to their subsequent delivery and are more likely to terminate reproduction completely, especially after male—male twins (Lummaa, 2001).

 Life-history theory, reproduction and longevity in humans

Fig. 27.1 (A) Survival and (B) predicted probability of dying from an infectious disease in pre-industrial Finnish mothers as a function of age at first reproduction for mothers of twins (grey line) and singletons (black line). The analyses control for the mothers' total number of offspring, social class and geographic and temporal differences in mortality. Note that mothers of singletons in panel B appeared to have higher risk of dying from infectious disease if they started reproduction after age 32, however this has little impact given that virtually all mothers (>90%) had their first birth before this age. Reproduced with permission from Helle et al. (2004).

First, mothers who give birth to twins have a higher risk of dying at childbirth (Haukioja et al., 1989; Gabler and Voland, 1994; McDermott et al., 1995). Second, in pre-industrial Finland when rates of fertility and mortality were high and effective healthcare was unavailable, mothers who increased their reproductive effort by delivering twins had 39% higher hazard of death after age 65 years, and consequently reduced post-reproductive lifespan, compared to mothers who produced only singletons during their lifetime (Figure 27.1A; Helle et al., 2004). This was true irrespective of the social class or (p. 402) wealth available to the mothers, and controlling for other reproductive traits such age at first reproduction and total family size and sex ratio. Similarly, rural Gambian mothers delivering twins had a 3.5-fold increase in mortality rates after menopause compared to mothers that had produced singletons only during their lifetimes (R. Sear, unpublished results).

Although the theoretical background for this kind of life-history trade-off between reproductive effort and survival is well established, there is surprisingly little information about the underlying mechanism mediating such costs of reproduction (Zera and Harshman, 2001; Barnes and Partridge, 2003). One prominent hypothesis proposed in animals is that reproductive effort may impair immune function against different pathogens by promoting immunosenescence (reviewed in Sheldon and Verhulst, 1996). The most compelling evidence for this hypothesis comes from the immunological studies in birds, which have demonstrated lowered humoral and cell-mediated responses to antigens as a consequence of experimentally elevated reproductive effort (Gustafsson et al., 1994; Sheldon and Verhulst, 1996; Lochmiller and Deerenberg, 2000; Norris and Evans, 2000; Lozano and Lank, 2003). In addition, increases in reproductive effort can impair immune function in the long term (Ardia et al., 2003), an effective immune system itself may be costly to maintain (Sheldon and Verhulst, 1996; Lochmiller and Deerenberg, 2000), and may constrain individual reproductive decisions. These kinds of mechanisms may also be in play in humans, but demonstrating that high reproductive effort accelerates immunosenescence would require one to establish a link between reproductive effort and impairment of immune function.

Findings in a study of pre-industrial Finnish twin mothers suggest that their reduced longevity might have been due to accelerated immunosenescence (Helle et al., 2004). Post-reproductive mothers of twins had a seven times higher risk of dying of an infectious disease (mainly tuberculosis) compared to mothers of singletons (Figure 27.1B). In eighteenth- and nineteenth-century Finland, as elsewhere in Europe, tuberculosis was common and many were infected with the disease early in life and carried it dormant for long periods of time before developing acute symptoms if the immune system became compromised (Flynn and Chan, 2001; Rajagopalan, 2001). The risk of dying of an infectious disease for Finnish mothers seemed to be particularly pronounced in mothers of twins after age 65 years (Helle et al., 2004), which corresponds well to the survival (p. 403) curves shown in Figure 27.1A. Young ages at first reproduction seemed to further increase the risk of succumbing to an infectious disease, suggesting that early reproductive effort may also have been relevant for the expression of immunosenescence when mothers produced twins. As mothers of twins did not show higher infection-related mortality during their reproductive ages compared to mothers of singletons, it is possible to exclude the alternative explanation that twinning was more frequent among those women who generally expressed lower levels of immune defence. One possibility is that twin births may be related to elevated maternal stress levels (Salami et al., 2003), which might have a negative bearing on maternal immunocompetence, and thus on their long-term survival (Buchanan, 2000).

27.2.2.2. Effects of producing sons versus daughters on maternal survival

Another way in which the reproductive effort of mothers for a given reproductive event may increase is when the investment is biased into production of offspring of the more expensive sex. In humans, sons are physiologically more demanding to produce than daughters, as indicated by their faster intrauterine growth rate (Marsál et al., 1996), heavier birth weight (Hoffman et al., 1974; Loos et al., 2001), and the longer time it takes mothers producing sons to reproduce again (Mace and Sear, 1997). The production of large and strongly male-biased families is predicted to be detrimental to maternal longevity in sexually size-dimorphic species in which males are larger (Kirkwood and Rose, 1991), although the resources available may modify such costs.

 Life-history theory, reproduction and longevity in humans

Fig. 27.2 Maternal post-reproductive (beyond age 50) survival in historical Sami mothers as a function of the number of sons produced over a lifetime. Reproduced with permission from Helle et al. (2002).

In line with this prediction, both historical mothers and contemporary mothers who bias their reproductive investment towards sons have reduced longevity compared to those producing a similar bias of daughters (Beise and Voland, 2002; Helle et al., 2002; van de Putte et al., 2004; Hurt et al., 2006). For example, in a study on historical reindeer-herding nomadic Sami of Northern Scandinavia, every son born was found to reduce maternal longevity on average by 34 weeks, whereas having daughters had a positive effect on maternal longevity (Figure 27.2; Helle et al., 2002). These findings suggest that giving birth to sons poses a higher relative long-term survival cost for mothers than giving birth to and raising daughters. This gender bias may be due to the lower direct physiological costs of daughters in conjunction with a family system where daughters help their mothers in their everyday tasks. That males have a negative effect (p. 404) on maternal longevity, whereas daughters have a positive effect, clearly demonstrates why studies can fail to find the predicted negative relationship between investment and survival if only total family size is considered as investment. Therefore, both the direct effects of reproductive investment and the social effects of gender-biased family structure seem to be important determinants of female lifespan in Sami.

Again, consistent with the immunosuppressive idea, one potential mechanism for the negative effects of biasing reproductive investment into production of more expensive sons on lifespan could be the greater loss of resources required to maintain effective immune defences (Sheldon and Verhulst, 1996; Lochmiller and Deerenberg, 2000). One possibility is that interactions between reproductive costs and sex-specific hormones influence maternal immune function and susceptibility to succumbing to infectious diseases. In primates, high concentrations of maternal testosterone can correlate with an excess of male offspring and high concentrations of maternal oestrogens with an excess of female offspring (Meulenberg and Hofman, 1991; Manning et al., 2002; Altmann et al., 2004; Perret, 2005). These hormones also influence maternal immune function: testosterone having negative effects on immunocompetence and estrogens having positive effects (Klein, 2000).

27.3. Benefits of a long life: reproductive and post-reproductive trade-offs

So far we have seen that increasing current reproductive effort may reduce future reproductive success as well as post-reproductive survival rates. Life-history theory would generally predict that negative relations between reproductive effort and post-reproductive survival should be of no evolutionary consequence, since there should be no selection for living beyond one's reproductive years. In addition, given that the selective forces acting on reproductive effort decline with age (Medawar, 1952; Hamilton, 1966), any selection acting on post-reproductive longevity would be predicted to be weak. Despite this, in humans, there is clearly some selection acting on post-reproductive survival, and this selection appears to be significant enough to allow women to survive for fully one-third of their life as a post-reproductive.

That women experience menopause, a complete and apparently irreversible physiological shut-down of reproductive potential, and then survive for a substantial amount of time thereafter has been the subject of much debate for decades (Pavelka and Fedigan, 1991; Marlowe, 2000; Peccei, 2001a, b; Hawkes, 2003; Lee, 2003). One reason for this debate is that menopause is not only an extreme life-history event, but would appear to be paradoxical from an evolutionary point of view. Another reason is that the selective benefits of menopause cannot be tested, for all women experience it; we will never know whether in our evolutionary past, women experiencing menopause produced significantly more and/or superior offspring than women who continued to reproduce until death.

One possibility is that menopause has itself been under selection (Peccei, 2001a, b). This could arise if the benefits of reproducing late in life are small (Medawar, 1952) while the costs are large (Williams, 1957; Peccei, 2001a). The benefits of reproducing late may be small because pregnancies in old age have an elevated risk of miscarriage, the foetus of older mothers has a higher risk of being born dead (Wood, 1994), having a defect (Gaulden, 1992) or being born small (Jolly et al., 2000). In addition, late reproduction may be costly, for a mother that dies during or shortly after childbirth will not only jeopardize the life of her current child, but also those of earlier children which are still dependent on their mother for sustenance and protection (Williams, 1957; Peccei, 2001). This problem is likely to be more acute in humans than most animals, for human offspring have a long period of dependence and inter-birth intervals are short and so several dependent offspring exist at any one time. Nevertheless, it could be argued that increased probabilities of birth defects late in life are merely a consequence of the onset of menopause rather than the cause.

Other empirical findings would also appear to be at odds with the above idea. First, women reproducing late in life (mid—late 40s) may produce more offspring than those that terminate reproduction early (late 30s—early 40s). For example, in the eighteenth and nineteenth centuries, (p. 405) Scandinavian Sami, which were reliant on reindeer herding and fishing and which lacked either medical care or contraceptives, produced more surviving children in their lifetime if they continued childbearing into their late 40s (Helle et al., 2005). Indeed, age at last reproduction explained 28% of the variance in offspring numbers, suggesting a key positive effect of age at last reproduction on evolutionary fitness. One explanation for this may be that in family-living species, the death of a mother may have a lower impact on offspring mortality than is often supposed because other relatives (husband, older siblings, grandparents, aunts/uncles, cousins) can subsume the role of a dead mother. Second, there is little evidence to suggest that humans terminate reproduction early in comparison to other primates when differences in body size are accounted for (Schultz, 1969; see Section 27.1).

An alternative explanation is that it has been lifespan that has been under evolutionary selection and that menopause is merely a by-product of more rapid phenotypic changes in lifespan than egg number. If mothers can increase the reproductive success of their offspring by helping with child care, then a woman with genes for living beyond her decline in fertility may produce more grandchildren (and hence forward more genes to the following generation) than a woman who died before being able to help her offspring to reproduce. It may be noteworthy to point out that a woman's termination of reproduction tends to coincide with the onset of her first offspring's reproductive career and so only a small increase in the lifespan of a ‘helping’ mother would have the potential to lead to fast evolutionary benefits. Nevertheless, that the age of menopause is variable, has a heritable genetic component (Kirk et al., 2001; van Asselt et al., 2004; Murabito et al., 2005; Pettay et al., 2005) and is caused by ‘destruction’ of eggs rather than a lack of them (Peccei, 2001b), suggests that menopause is unlikely to be a mere by-product of selection on longevity. Consequently, our best guess at present is that both menopause (see above) and longevity (see below) have been (and are) under evolutionary selection.

Whether it has been menopause and/or lifespan that has been under selection, there is now compelling evidence to suggest that post-reproductive women can indeed have a significant and positive effect on their offspring's reproductive success. In rural Gambia, the presence of a grandmother improves the dietary condition of grandchildren and increases their survival chances (Sear et al., 2000). Among the Hadza hunter-gatherers of Tanzania, variation in child weight is positively correlated with grandmother's foraging time (Hawkes et al., 1997), while in historical populations of Germany (Voland and Beise, 2002) and Japan (Jamison, 2002), the maternal grandmothers improved the survival of grandchildren. Finally, Lahdenperä et al., (2004) showed that mothers gained significant fitness by surviving beyond menopause. They found that in farming/fishing communities of pre-modern (eighteenth and nineteenth centuries) Finnish and Canadian people, women gained two extra grandchildren for every 10 years they survived beyond menopause until their mid-70s, showing that lifespan can be under positive selection at least until this age (Figure 27.3). This effect arose because offspring in the presence of their post-reproductive mothers bred earlier, more frequently, for longer and more successfully. These effects were common to sons and daughters, rich and poor and in predictable and unpredictable food areas, showing that post-reproductive mothers can influence their offspring irrespective of which sex is philopatric and irrespective of habitat quality.

 Life-history theory, reproduction and longevity in humans

Fig. 27.3 Female post-reproductive lifespan and total number of grandchildren contributed to the following generation in (A) pre-industrial Finland and (B) pre-industrial Canada. Graphs show predicted means (±1 SE), after controlling for effects of social class, population (Finland) and birth cohort (Finland and Canada). Reproduced with permission from Lahdenperä et al. (2004).

While animals appear to show no identical analogue to human post-reproductive mothers, it is useful to point out that some similarities do exist. First, in eusocial insects, the majority of individuals in a colony are sterile and their sole purpose in life is to increase the reproductive success of their mother. Thus the link between sterility and helping relatives has an equivalent in the animal kingdom, although in this case it is offspring helping mothers rather than the other way around (Foster and Ratnieks, 2005). Second, in cooperatively breeding birds and mammals, although parents are fertile, it is not uncommon for them to help their offspring breed, either because mothers have failed in their own breeding attempt or because offspring and mothers co-breed (Dickinson and Hatchwell, 2004; Russell, 2004). It may not require a major evolutionary leap for ageing (p. 406) mothers to wholly concede reproduction to a daughter (or a son's wife) if competition for resources is intense and the reproductive output/success of younger offspring (aided by the mother) is substantially greater than their own. Nor need it necessarily require a major evolutionary leap for mothers to shut down their reproductive system, if by so doing they can reduce competition with their offspring and prolong their own lifespan.

Thus, because women accrue fitness during both reproductive and post-reproductive phases, this means that the reproductive success gained prior to menopause represents only a proportion of total fitness. This has implications regarding optimal fitness-maximizing tactics, rates of senescence and lifespan in humans. In most animals, individual fitness is maximized by optimizing the trade-off between current and future reproduction, with the amount of selection on early reproduction relative to late reproduction influencing, in part, the rate at which individuals senesce and die. However, increasing current reproductive effort by humans not only reduces future reproductive success but also their post-reproductive survival rates (see above), suggesting that high investment in a reproductive attempt not only has a negative effect on the ability to invest in future reproductive attempts but also on the ability to invest following menopause. Consequently, fitness in humans may be maximized by optimization of trade-offs both within the reproductive and between the reproductive and post-reproductive phases. This leads to the intriguing likelihood that humans suffer from both reproductive and post-reproductive senescence with the relative importance of fitness accrued during each phase influencing ultimate lifespan.

However, it is currently largely unknown how early reproductive effort influences rates of reproductive senescence, or how reproductive effort overall affects rates of post-reproductive senescence. Previous research has typically identified the factors that influence ‘fitness’ either before or after menopause and has generally failed to combine the two or to consider how fitness gained during reproduction influences fitness gained after reproduction. In addition, it is currently unknown how reproductive tactics interact with ecology and demography to influence overall fitness and rates or types of reproductive and post-reproductive senescence. Investigations along some of these avenues are likely to be an exciting and fruitful direction for future research.

27.4. Heritability, genetic constraints and evolutionary trade-offs

We have seen that increase in reproductive effort may be beneficial as it leads to the production of (p. 407) more and/or better quality offspring, but that such increases in investment into current reproduction may be detrimental for maternal future reproductive success and longevity. We have also seen how, in humans, high investment during reproduction attempts may compromise a woman's ability to invest in the reproductive attempts of her offspring following menopause. Finally, we have seen that women can accrue fitness during both reproductive and post-reproductive phases, and hence fitness in humans is maximised by optimization of tradeoffs both within the reproductive and between the reproductive and post-reproductive phases. The questions are: are life-history traits under genetic control, and what constrains the evolution of both high reproductive effort and long lifespan?

Because the premises of organic evolution involve genetic variability and heritability in different life-history traits, the most fruitful way to investigate associations among life-history traits is by estimating genetic correlations between traits from sibling analysis, or from selection experiments, and not from phenotypic correlations (Reznick, 1985, 1992). However, conclusions of most human life-history studies to date have been based on the phenotypic correlations without information on the underlying genetic components or correlations. Such studies are unable to determine the evolutionary response to selection on the traits studied. Yet from an evolutionary point of view, phenotypic correlations are particularly interesting only if they have a genetic basis, since natural selection can only lead to an evolutionary response when it acts on a heritable character. Unfortunately, estimating heritability of human life-history traits is problematic. First, obtaining data from humans that allows an estimation of heritabilities and genetic correlations for life-history traits is difficult. Second, effects of a common environment shared by close relatives and cultural transmission can inflate estimates of heritability. A lack of information on the heritability and genetic constraints of reproductive traits in human populations has resulted in a limited understanding of whether the phenotypic selection documented could lead to evolutionary changes over time.

There are some recent exceptions that provide interesting insights into the evolution of life-history traits. First, Kirk et al. (2001) used a twin-study design to calculate heritabilities for a set of life-history traits in a contemporary Australian population. Second, Pettay et al. (2005) used pedigree records of pre-industrial Finns using a maximum-likelihood (REML)-based technique and an ‘animal model’. This latter methodology controls for common environmental effects and considers the similarity between pairs of individuals that vary in their degree of relatedness and for whom shared environments are less problematic (Falconer and Mackay, 1996; Lynch and Walsh, 1998; Kruuk, 2004).

In both contemporary Australian and rural historical Finnish women, the key female life-history traits, such as age at menarche and menopause, reproductive rate and longevity, had significant additive genetic heritability, potentially permitting rapid evolutionary responses to selection (Kirk et al., 2001; Pettay et al., 2005). Furthermore, in both populations, there was also substantial heritable variation in fitness itself: in Finns 47% and in Australians 39% of the variance in fitness was attributable to additive genetic effects (the remainder of the variation in the Australians, for example, consisting of unique environmental effects and small effects from education and religion). However, there were also considerable genetic constraints between reproductive traits and longevity (negative genetic trade-offs), which are usually considered fundamental for life-history trait optimization by natural selection. For example, in the Finns, there were significant negative genetic correlations between age at first reproduction and longevity, and the mean inter-birth interval and longevity (Pettay et al., 2005). Their existence implies that females who started reproducing early, or had short inter-birth intervals, had relatively shorter lifespans too, supporting the hypothesis that rate of reproduction should trade-off with longevity (Williams, 1957; Kirkwood, 1977; Kirkwood and Rose, 1991). This type of negative additive genetic correlation, or antagonistic pleiotropy, is often expected for fitness components, and may be one force maintaining additive genetic variation in nature (Falconer and Mackay, 1996), although it may generally be rare in natural populations (Kruuk, 2004).

(p. 408) These trade-offs may have had important implications for the evolution of human life-history, given that human females may gain fitness benefits through outliving their own reproductive capacity by improving the reproductive success of their offspring and the survival of their grand-offspring. Such positive fitness effects of post-reproductive survival would intensify selection for genes increasing longevity, but the negative genetic correlations between measures of reproductive rate and longevity set constrains on any response to such selection imposed by countervailing selection favouring early or frequent breeding (Käär et al., 1996). The correlations are also interesting since they suggest some underlying genetic mechanism affecting the starting age of reproduction and longevity, and rate of reproduction and longevity. The relatively large additive genetic variance and genetic constraints between key life-history traits that both studies found suggest that in these populations, human life-history certainly has had the potential to evolve by optimizing natural selection, as classical life-history theory predicts. The significance of the maternal effects, e.g. for female age at first reproduction in Finns (Pettay et al., 2005), further emphasizes that social aspects, like wealth of the family, also play an important role in human life-history evolution. Studies showing how phenotypic selection gradients translate into genetic responses to selection in different human populations are an essential and much-needed direction for future research.

27.5. Synthesis and future directions

Human life-history evolution is a fascinating subject and substantial advancements to our understanding of how our life-history compares and contrasts with that of animals have been made over the past decades. Humans are a problematic study species for many life-history questions because manipulative experiments, which have been highly illuminating in similar studies of animals, are out of the question and because culture has a strong influence on reproductive patterns. Nevertheless, humans have some substantial advantages, too. First, not surprisingly, findings of human studies are of broad interest to scientists and lay-peoples alike. Second, the medical literature on humans, although often under-used by those interested in life-history evolution, allows significant insights into the mechanism driving life-history trade-offs. Third, the ability to follow the fate of virtually all dispersing individuals in some human populations over several generations allows a better estimation of the effects of life-history strategies on evolutionary fitness than for most wild vertebrates.

Life-history theory was developed for animals. The available evidence clearly demonstrates that such theory is highly applicable to humans. For example, offspring quality/quantity tradeoffs and trade-offs between current and future reproduction have been documented in humans (Mace and Sear, 1997; Lummaa et al., 1998, 2001). In addition, in both animals and humans, demonstrating a trade-off between reproductive investment and longevity has proved to be inherently difficult, presumably because mothers of high quality are both more able to invest heavily in reproduction and to survive for a long time (Clutton-Brock, 1991). While animal studies can often reduce this problem by manipulating reproductive effort, the inability to manipulate reproductive investment in humans further reduces our ability to test for trade-offs between reproductive investment and longevity. That most studies in humans actually report a positive correlation between investment and longevity is testament to the problem of confounding influences of maternal quality. Future studies investigating such relationships must be acutely aware of this and would benefit substantially by endeavouring to circumvent the obvious problems. The use of multivariate statistics, which allow one to control for the many potential confounding influences, is essential. Potentially confounding influences include: maternal age, previous investment (e.g. number, delivery type, sex, survival, inter-birth interval of previous offspring) and resource availability. Furthermore, an appreciation of the difference between producing offspring at the same time versus at different times and the potentially contrasting effects of producing sons versus daughters on maternal survival are also potentially of critical importance.

An area of human life-history evolution that has been almost wholly devoid of attention is (p. 409) the unified area of heritability and selection, despite being at the core of the whole field. For selection to influence the life-history trait of an individual, that trait must have a heritable genetic component. Moreover, for variation in the trait to be potentially receptive to selection, one must be able to demonstrate additive genetic variance associated with the trait. The majority of the few attempts made to investigate such possibilities have used phenotypic correlations. Estimating heritabilities and genetic correlations for life-history traits is complicated by the fact that our estimations of heritability can be inflated by shared family effects and cultural transmission within genetic lineages. While comparisons of twins have some advantages (Kirk et al., 2001), an alternative method, and that which is most commonly adopted in animal studies, is to use residual maximum likelihood methods and an ‘animal model’ which can control for shared family effects (Kruuk, 2004).

In conclusion, theoretical models developed to explain life histories in animals and previous empirical tests in humans have led to a significant advancement in our understanding of the evolution of human life histories. However, we are far from a complete understanding. Armed with the findings over the past few decades and recent analytical advancements for estimating fitness, heritability, selection and rates of senescence, the field of human life-history evolution is at an enthralling stage of its own evolution.

Acknowledgments

I thank Andy Russell, Charlotte Faurie and Ian Rickard for constructive comments and suggestions made on earlier drafts of this chapter; Samuli Helle, Mirkka Lahdenperä and Jenni Pettay for collaboration on the Finnish and Sami people; Terho Koira for continuous help; and the Royal Society of London for financial support.

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