Virpi Lummaa

Fitness benefits of prolonged post-reproductive lifespan in women

Most animals reproduce until they die, but in humans, females can survive long after ceasing reproduction. In theory, a prolonged post-reproductive lifespan will evolve when females can gain greater fitness by increasing the success of their offspring than by continuing to breed themselves. Although reproductive success is known to decline in old age, it is unknown whether women gain fitness by prolonging lifespan post-reproduction. Using complete multi-generational demographic records, we show that women with a prolonged post-reproductive lifespan have more grandchildren, and hence greater fitness, in pre-modern populations of both Finns and Canadians. This fitness benefit arises because post-reproductive mothers enhance the lifetime reproductive success of their offspring by allowing them to breed earlier, more frequently and more successfully. Finally, the fitness benefits of prolonged lifespan diminish as the reproductive output of offspring declines. This suggests that in female humans, selection for deferred ageing should wane when ones own offspring become post-reproductive and, correspondingly, we show that rates of female mortality accelerate as their offspring terminate reproduction.

Early development, survival and reproduction in humans

Environmental factors commonly influence the growth and early development of individuals in wild populations of mammals. Such influences can exert downstream effects on the phenotypic quality and breeding success of the same individuals in adulthood, as well as on the growth and subsequent reproductive success of their offspring. Recent studies of humans indicate that similar effects occur both in Western human populations and in human populations subject to nutritional stress. Here, we compare evidence for the effects of early development on growth, survival and breeding performance in humans to similar trends in food-restricted populations of other mammals. We highlight the relevance of findings from animal studies to humans and vice versa, and suggest that the integration of wild animal and human studies could increase our knowledge about how early development shapes reproductive performance across generations.

Evolution of sex differences in lifespan and aging: Causes and constraints

Why do the two sexes have different lifespans and rates of aging? Two hypotheses based on asymmetric inheritance of sex chromosomes (“unguarded X”) or mitochondrial genomes (“mothers curse”) explain sex differences in lifespan as sex‐specific maladaptation leading to increased mortality in the shorter‐lived sex. While asymmetric inheritance hypotheses equate long life with high fitness, considerable empirical evidence suggests that sexes resolve the fundamental tradeoff between reproduction and survival differently resulting in sex‐specific optima for lifespan. However, selection for sex‐specific values in life‐history traits is constrained by intersexual genetic correlations resulting in intra‐locus sexual conflict over optimal lifespan. The available data suggest that the evolution of sexual dimorphism only partially resolves these conflicts. Sexual conflict over optimal trait values, which has been demonstrated in model organisms and in humans, is likely to play a key role in shaping the evolution of lifespan, as well as in maintaining genetic variation for sex‐specific diseases.

Does the contraceptive pill alter mate choice in humans

Female and male mate choice preferences in humans both vary according to the menstrual cycle. Women prefer more masculine, symmetrical and genetically unrelated men during ovulation compared with other phases of their cycle, and recent evidence suggests that men prefer ovulating women to others. Such monthly shifts in mate preference have been suggested to bring evolutionary benefits in terms of reproductive success. New evidence is now emerging that taking the oral contraceptive pill might significantly alter both female and male mate choice by removing the mid-cycle change in preferences. Here, we review support for such conclusions and speculate on the consequences of pill-induced choice of otherwise less-preferred partners for relationship satisfaction, durability and, ultimately, reproductive outcomes.

When fecundity does not equal fitness: evidence of an offspring quantity versus quality trade-off in pre-industrial humans

Maternal fitness should be maximized by the optimal division of reproductive investment between offspring number and offspring quality. While evidence for this is abundant in many taxa, there have been fewer tests in mammals, and in particular, humans. We used a dataset of humans spanning three generations from pre-industrial Finland to test how increases in maternal fecundity affect offspring quality and maternal fitness in contrasting socio-economic conditions. For ‘resource-poor’ landless families, but not ‘resource-rich’ landowning families, maternal fitness returns diminished with increased maternal fecundity. This was because the average offspring contribution to maternal fitness declined with increased maternal fecundity for landless but not landowning families. This decline was due to reduced offspring recruitment with increased maternal fecundity. However, in landowning families, recruited offspring fecundity increased with increased maternal fecundity. This suggests that despite decreased offspring recruitment, maternal fitness is not reduced in favourable socio-economic conditions due to an increase in subsequent offspring fecundity. These results provide evidence consistent with an offspring quantity–quality trade-off in the lifetime reproduction of humans from poor socio-economic conditions. The results also highlight the importance of measuring offspring quality across their whole lifespan to estimate reliably the fitness consequences of increased maternal fecundity.

Maternal effects in cooperative breeders: from hymenopterans to humans

The environment that an offspring experiences during its development can have lifelong consequences for its morphology, anatomy, physiology and behaviour that are strong enough to span generations. One aspect of an offsprings environment that can have particularly pronounced and long-lasting effects is that provided by its parent(s) (maternal effects). Some disciplines in biology have been quicker to appreciate maternal effects than others, and some organisms provide better model systems for understanding the causes and consequences of the maternal environment for ecology and evolution than others. One field in which maternal effects has been poorly represented, and yet is likely to represent a particularly fruitful area for research, is the field of cooperative breeding (i.e. systems where offspring are reared by carers in addition to parent(s)). Here, we attempt to illustrate the scope of cooperative breeding systems for maternal effects research and, conversely, highlight the importance of maternal effects research for understanding cooperative breeding systems. To this end, we first outline why mothers will commonly benefit from affecting the phenotype of their offspring in cooperative breeding systems, present potential strategies that mothers could employ in order to do so and offer predictions regarding the circumstances under which different types of maternal effects might be expected. Second, we highlight why a neglect of maternal strategies and the effects that they have on their offspring could lead to miscalculations of helper/worker fitness gains and a misunderstanding of the factors selecting for the evolution and maintenance of cooperative breeding. Finally, we introduce the possibility that maternal effects could have significant consequences for our understanding of both the evolutionary origins of cooperative breeding and the rise of social complexity in cooperative systems.

Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women

Evolutionary theory of senescence emphasizes the importance of intense selection on early reproduction owing to the declining force of natural selection with age that constrains lifespan. In humans, recent studies have, however, suggested that late-life mortality might be more closely related to late rather than early reproduction, although the role of late reproduction on fitness remains unclear. We examined the association between early and late reproduction with longevity in historical post-reproductive Sami women. We also estimated the strength of natural selection on early and late reproduction using path analysis, and the effect of reproductive timing on offspring survival to adulthood and maternal risk of dying at childbirth. We found that natural selection favoured both earlier start and later cessation of reproduction, and higher total fe cundity. Maternal age at childbirth was not related to offspring or maternal survival. Interestingly, females who produced their last offspring at advanced age also lived longest, while age at first reproduction and total fecundity were unrelated to female longevity. Our results thus suggest that reproductive and somatic senescence may have been coupled in these human populations, and that selection could have favoured late reproduction. We discuss alternative hypotheses for the mechanisms which might have promoted the association between late reproduction and longevity.

Natural Selection on Female Life-History Traits in Relation to Socio-Economic Class in Pre-Industrial Human Populations

Life-history theory predicts that resource scarcity constrains individual optimal reproductive strategies and shapes the evolution of life-history traits. In species where the inherited structure of social class may lead to consistent resource differences among family lines, between-class variation in resource availability should select for divergence in optimal reproductive strategies. Evaluating this prediction requires information on the phenotypic selection and quantitative genetics of life-history trait variation in relation to individual lifetime access to resources. Here, we show using path analysis how resource availability, measured as the wealth class of the family, affected the opportunity and intensity of phenotypic selection on the key life-history traits of women living in pre-industrial Finland during the 1800s and 1900s. We found the highest opportunity for total selection and the strongest selection on earlier age at first reproduction in women of the poorest wealth class, whereas selection favoured older age at reproductive cessation in mothers of the wealthier classes. We also found clear differences in female life-history traits across wealth classes: the poorest women had the lowest age-specific survival throughout their lives, they started reproduction later, delivered fewer offspring during their lifetime, ceased reproduction younger, had poorer offspring survival to adulthood and, hence, had lower fitness compared to the wealthier women. Our results show that the amount of wealth affected the selection pressure on female life-history in a pre-industrial human population.

Natural and sexual selection in a monogamous historical human population

Whether and how human populations exposed to the agricultural revolution are still affected by Darwinian selection remains controversial among social scientists, biologists, and the general public. Although methods of studying selection in natural populations are well established, our understanding of selection in humans has been limited by the availability of suitable datasets. Here, we present a study comparing the maximum strengths of natural and sexual selection in humans that includes the effects of sex and wealth on different episodes of selection. Our dataset was compiled from church records of preindustrial Finnish populations characterized by socially imposed monogamy, and it contains a complete distribution of survival, mating, and reproductive success for 5,923 individuals born 1760–1849. Individual differences in early survival and fertility (natural selection) were responsible for most variation in fitness, even among wealthier individuals. Variance in mating success explained most of the higher variance in reproductive success in males compared with females, but mating success also influenced reproductive success in females, allowing for sexual selection to operate in both sexes. The detected opportunity for selection is in line with measurements for other species but higher than most previous reports for human samples. This disparity results from biological, demographic, economic, and social differences across populations as well as from failures by most previous studies to account for variation in fitness introduced by nonreproductive individuals. Our results emphasize that the demographic, cultural, and technological changes of the last 10,000 y did not preclude the potential for natural and sexual selection in our species.

Male twins reduce fitness of female co-twins in humans

In mammals, including humans, female fetuses that are exposed to testosterone from adjacent male fetuses in utero can have masculinized anatomy and behavior. However, the reproductive consequences of such prebirth sex-ratio effects for offspring and their implications for maternal fitness remain unexplored. Here we investigate the effects of being gestated with a male co-twin for daughter lifetime reproductive success, and the fitness consequences for mothers of producing mixed-sex twins in preindustrial (1734–1888) Finns. We show that daughters born with a male co-twin have reduced lifetime reproductive success compared to those born with a female co-twin. This reduction arises because such daughters have decreased probabilities of marrying as well as reduced fecundity. Mothers who produce opposite-sex twins consequently have fewer grandchildren (and hence lower fitness) than mothers who produce same-sex twins. Our results are unlikely to be a consequence of females born with male co-twins receiving less nutrition because such females do not have reduced survival and increases in food availability fail to improve their reproductive success. Nor are our results explained by after-birth social factors (females growing up with similarly aged brothers) because females born with a male co-twin have reduced success even when their co-twin dies shortly after birth and are raised as singletons after birth. Our findings suggest that hormonal interactions between opposite-sex fetuses known to influence female morphology and behavior can also have negative effects on daughter fecundity and, hence, maternal fitness, and bear significant implications for adaptive sex allocation in mammals.