Samuli Helle

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.

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.

Female field voles with high testosterone and glucose levels produce male-biased litters

The proximate physiological mechanisms producing the parental ability to vary offspring sex ratio in many vertebrates remain elusive. Recently, high concentrations of maternal testosterone and glucose and low concentrations of maternal corticosterone have been suggested to explain male bias in offspring sex ratio. We examined how these factors affect secondary offspring sex ratio in nondomesticated field voles, Microtus agrestis, while controlling for maternal age, testosterone level of the male and body condition of both the female and the male. We found that females with high preconception serum testosterone and glucose levels produced a male-biased litter, whereas there was no association between maternal corticosterone level and litter sex ratio. Older females produced a bias towards sons, but neither their body condition nor paternal testosterone level correlated with litter sex ratio. Finally, females mated with a high body-condition male tended to deliver a male-biased litter. Our results suggest that several physiological traits of the mother may simultaneously be related to offspring sex ratio in mammals.

Carotenoid Composition of Invertebrates Consumed by Two Insectivorous Bird Species

Dietary carotenoids are important pigments, antioxidants, and immune-stimulants for birds. Despite recent interest in carotenoids in bird ecology, we know surprisingly little about the carotenoid content of invertebrates consumed by birds. We compared carotenoid (lutein, β-carotene, and total) concentrations in invertebrates brought to nestlings by two insectivorous passerines, the great tit, Parus major and the pied flycatcher, Ficedula hypoleuca. We also compared carotenoid levels between environments that were either polluted by heavy metals or were not polluted, because the carotenoid-based plumage color of P. major nestlings is affected by environmental pollution. Lepidopterans were the most carotenoid-rich food items and contained the largest proportion of lutein. There were no differences in carotenoid concentrations in the food items of the two bird species but P. major nestlings obtained more carotenoids from their invertebrate diet than F. hypoleuca nestlings because the P. major diet had a higher proportion of lepidopteran larvae. In polluted areas, P. major nestlings consumed lower levels of dietary carotenoids than in unpolluted areas because of temporal differences in caterpillar abundance between polluted and unpolluted sites. Our study suggests that pollution-related difference in nestling plumage color in P. major is related to varying dietary proportion of lutein-rich food items rather than pollution-related variation in insect carotenoid levels.

Temperature-related birth sex ratio bias in historical Sami: warm years bring more sons.

The birth sex ratio of vertebrates with chromosomal sex determination has been shown to respond to environmental variability, such as temperature. However, in humans the few previous studies on environmental temperature and birth sex ratios have produced mixed results. We examined whether reconstructed annual mean temperatures were associated with annual offspring sex ratio at birth in the eighteenth to nineteenth century Sami from northern Finland. We found that warm years correlated with a male-biased sex ratio, whereas a warm previous year skewed sex ratio towards females. The net effect of one degree Celsius increase in mean temperature during these 2 years corresponded to approximately 1% more sons born annually. Although the physiological and ecological mechanisms mediating these effects and their evolutionary consequences on parental fitness remain unknown, our results show that environmental temperature may affect human birth sex ratio.

Food availability at birth limited reproductive success in historical humans

Environmental conditions in early life can profoundly affect individual development and have consequences for reproductive success. Limited food availability may be one of the reasons for this, but direct evidence linking variation in early-life nutrition to reproductive performance in adulthood in natural populations is sparse. We combined historical agricultural data with detailed demographic church records to investigate the effect of food availability around the time of birth on the reproductive success of 927 men and women born in 18th-century Finland. Our study population exhibits natural mortality and fertility rates typical of many preindustrial societies, and individuals experienced differing access to resources due to social stratification. We found that among both men and women born into landless families (i.e., with low access to resources), marital prospects, probability of reproduction, and offspring viability were all positively related to local crop yield during the birth year. Such effects were generally absent among those born into landowning families. Among landless individuals born when yields of the two main crops, rye and barley, were both below median, only 50% of adult males and 55% of adult females gained any reproductive success in their lifetime, whereas 97% and 95% of those born when both yields were above the median did so. Our results suggest that maternal investment in offspring in prenatal or early postnatal life may have profound implications for the evolutionary fitness of human offspring, particularly among those for which resources are more limiting. Our study adds support to the idea that early nutrition can limit reproductive success in natural animal populations, and provides the most direct evidence to date that this process applies to humans.

Evolutionary ecology of human birth sex ratio under the compound influence of climate change, famine, economic crises and wars.

1. Human sex ratio at birth at the population level has been suggested to vary according to exogenous stressors such as wars, ambient temperature, ecological disasters and economic crises, but their relative effects on birth sex ratio have not been investigated. It also remains unclear whether such associations represent environmental forcing or adaptive parental response, as parents may produce the sex that has better survival prospects and fitness in a given environmental challenge. 2. We examined the simultaneous role of wars, famine, ambient temperature, economic development and total mortality rate on the annual variation of offspring birth sex ratio and whether this variation, in turn, was related to sex-specific infant mortality rate in Finland during 1865-2003. 3. Our findings show an increased excess of male births during the World War II and during warm years. Instead, economic development, famine, short-lasting Finnish civil war and total mortality rate were not related to birth sex ratio. Moreover, we found no association between annual birth sex ratio and sex-biased infant mortality rate among the concurrent cohort. 4. Our results propose that some exogenous challenges like ambient temperature and war can skew human birth sex ratio and that these deviations likely represent environmental forcing rather than adaptive parental response to such challenges.

SELECTION FOR INCREASED BROOD SIZE IN HISTORICAL HUMAN POPULATIONS

Abstract Human twinning rates are considered to either reflect the direct fitness effects of twinning in variable environments, or to be a maladaptive by‐product of selection for other maternal reproductive traits (e.g., polyovulation). We used historical data (1710‐1890) of Sami populations from Northern Scandinavia to contrast these alternative hypotheses. We found that women who produced twins started their reproduction younger, ceased it later, had higher lifetime fecundity, raised more offspring to adulthood, and had higher fitness (individual λ.) than mothers of singletons in all populations studied. For example, an average of 1.2 offspring survived to adulthood from a twin delivery, irrespective of its sex ratio, whereas only 0.8 offspring survived to adulthood from a singleton delivery. Only if mothers started reproduction at very late age (>37 yr), or had a very long reproductive life span (>20 yr), was it more beneficial to produce only singletons. These findings suggest that twin deliveries among Sami could not be explained as a maladaptive by‐product of selection for other maternal reproductive traits. In contrast, our results suggest that twinning was under natural selection, although the strength of selection was likely to have been context dependent.

Culled males, infant mortality and reproductive success in a pre-industrial Finnish population

Theoretical and empirical literature asserts that the sex ratio (i.e. M/F) at birth gauges the strength of selection in utero and cohort quality of males that survive to birth. We report the first individual-level test in humans, using detailed life-history data, of the ‘culled cohort’ hypothesis that males born to low annual sex ratio cohorts show lower than expected infant mortality and greater than expected lifetime reproductive success. We applied time-series and structural equation methods to a unique multigenerational dataset of a natural fertility population in nineteenth century Finland. We find that, consistent with culled cohorts, a 1 s.d. decline in the annual cohort sex ratio precedes an 8% decrease in the risk of male infant mortality. Males born to lower cohort sex ratios also successfully raised 4% more offspring to reproductive age than did males born to higher cohort sex ratios. The offspring result, however, falls just outside conventional levels of statistical significance. In historical Finland, the cohort sex ratio gauges selection against males in utero and predicts male infant mortality. The reproductive success findings, however, provide weak support for an evolutionarily adaptive explanation of male culling in utero.