Accelerated immunosenescence in preindustrial twin mothers

Helle, Samuli; Lummaa, Virpi; Jokela, Jukka

doi:10.1073/pnas.0402215101

Cited by 43 publications

(26 citation statements)

References 45 publications

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“…The physiological mechanisms underlying the impact of reproduction on parental longevity are unclear, although for women, they may be due to insufficient time to recover from the stress from the previous pregnancy (''maternal depletion syndrome'' hypothesis) (28). Pregnancy involves calcium loss and other nutritional deficits, oxidative stress, and reduced immunological resistance to infectious diseases (9,(29)(30)(31). Mothers stressed from rearing chronically ill children that require enormous investment have short telomeres for their age, suggesting oxidative stress and cellular senescence (32), but it is not known whether fathers incur similar effects.…”

Section: Discussionmentioning

confidence: 99%

“…Also, it is widely assumed that women have higher costs of reproduction than men because of enduring pregnancy, childbirth, and lactation, but evidence is lacking. Studies on women show that high parity and low birth spacing are associated with reduced health (9), postreproductive survival (10)(11)(12)(13), and offspring quality (14,15). There are only a few studies on men, and they suggest that men incur no fitness costs for reproduction (16,17).…”

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Differential fitness costs of reproduction between the sexes

Penn

Smith

2007

Proc. Natl. Acad. Sci. U.S.A.

154

116

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Natural selection does not necessarily favor maximal reproduction because reproduction imposes fitness costs, reducing parental survival, and offspring quality. Here, we show that parents in a preindustrial population in North America incurred fitness costs from reproduction, and women incurred greater costs than men. We examined the survivorship and reproductive success (Darwinian fitness) of 21,684 couples married between 1860 and 1895 identified in the Utah Population Database. We found that increasing number of offspring (parity) and rates of reproduction were associated with reduced parental survivorship, and significantly more for mothers than fathers. Parental mortality resulted in reduced survival and reproduction of offspring, and the mothers' mortality was more detrimental to offspring than the fathers'. Increasing family size was associated with lower offspring survival, primarily for later-born children, indicating a tradeoff between offspring quantity versus quality. Also, we found that the costs of reproduction increased with age more for women than men. Our findings help to explain some puzzling aspects of human reproductive physiology and behavior, including the evolution of menopause and fertility declines associated with improvements in women's status (demographic transitions).maternal depletion ͉ menopause ͉ reproductive effort ͉ biodemography ͉ life-history tradeoff T he idea that reproduction confers fitness costs and benefits is central to evolutionary life-history theory, and evidence for reproductive costs has been found in a variety of species (1-3), including humans (4, 5). The evidence in humans is mixed (6) and controversial (7,8), and so more studies would help to solve this important question. Also, it is widely assumed that women have higher costs of reproduction than men because of enduring pregnancy, childbirth, and lactation, but evidence is lacking. Studies on women show that high parity and low birth spacing are associated with reduced health (9), postreproductive survival (10-13), and offspring quality (14, 15). There are only a few studies on men, and they suggest that men incur no fitness costs for reproduction (16,17). Taken together, the evidence supports the idea that women incur greater reproductive costs than men. However, the studies on men were mainly conducted on aristocrats and industrial societies, and men in most societies probably have not been so sheltered from the costs of reproduction. Thus, more studies are needed, especially large, longitudinal studies on couples living in preindustrial societies. Our aim was to examine the fitness costs of reproduction for husbands versus wives in an historical, 19th-century population in North America facing resource limitations, because a previous study suggested that both sexes in this population incurred fitness costs for reproduction (12).Determining the relative costs of reproduction for the sexes is relevant to understanding the evolution of some puzzling aspects of human physiology and behavior. For example, menopa...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Differential fitness costs of reproduction between the sexes

Penn

Smith

2007

Proc. Natl. Acad. Sci. U.S.A.

154

116

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“…Based on previous studies examining links between early exposure to mortality and later-life health and fitness (19,(38)(39)(40), we aimed to estimate an individual's experience of infectious diseases in their first 5 y of life, as illustrated by the prevalence of death from infectious diseases recorded by the church (54). Because children and adults are vulnerable to different diseases in this population (SI Appendix, Tables S3 and S5), we recorded the number of individuals aged 0-10 y who were alive in the parish in each year, 1751-1855, a total of 194,182 person-y (SI Appendix, Table S2), during which time 4,780 children died of a known cause, 73% of which were due to infectious diseases (SI Appendix, Table S3); 22% of deaths were from an unknown disease, which we included in the infectious category.…”

Section: Methodsmentioning

confidence: 99%

Early-life disease exposure and associations with adult survival, cause of death, and reproductive success in preindustrial humans

Hayward

Rigby

Lummaa

2016

Proc. Natl. Acad. Sci. U.S.A.

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A leading hypothesis proposes that increased human life span since 1850 has resulted from decreased exposure to childhood infections, which has reduced chronic inflammation and later-life mortality rates, particularly from cardiovascular disease, stroke, and cancer. Early-life cohort mortality rate often predicts later-life survival in humans, but such associations could arise from factors other than disease exposure. Additionally, the impact of early-life disease exposure on reproduction remains unknown, and thus previous work ignores a major component of fitness through which selection acts upon life-history strategy. We collected data from seven 18th-and 19th-century Finnish populations experiencing naturally varying mortality and fertility levels. We quantified early-life disease exposure as the detrended child mortality rate from infectious diseases during an individual's first 5 y, controlling for important social factors. We found no support for an association between early-life disease exposure and all-cause mortality risk after age 15 or 50. We also found no link between early-life disease exposure and probability of death specifically from cardiovascular disease, stroke, or cancer. Independent of survival, there was no evidence to support associations between early-life disease exposure and any of several aspects of reproductive performance, including lifetime reproductive success and age at first birth, in either males or females. Our results do not support the prevailing assertion that exposure to infectious diseases in early life has long-lasting associations with later-life all-cause mortality risk or mortality putatively linked to chronic inflammation. Variation in adulthood conditions could therefore be the most likely source of recent increases in adult life span.inflammation | stress | infection | life history | fitness

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“…To aid the interpretation of the coefficients of the number of offspring of each sex in the presence of interactions, these variables were grand mean centred prior to analyses [21]. In women, we also controlled for whether they produced twins or not [22]. Assumptions of proportional hazards were examined by also fitting time-dependent coefficients of explanatory variables (i.e.…”

Section: (B) Statistical Analysesmentioning

confidence: 99%

A trade-off between having many sons and shorter maternal post-reproductive survival in pre-industrial Finland

Helle

Lummaa

2013

Biol. Lett.

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A bias in reproduction towards sons, which are energetically more costly than daughters, has been suggested to shorten parental lifespan, but previous results have been mixed. Reproductive costs should be most evident in low rather than high resource settings, and are not expected to be severe in men, because women pay higher direct costs of reproduction. We, therefore, used demographic data from pre-industrial Finland to investigate whether the number of sons and daughters born affected their parents' post-reproductive survival and whether this was related to parent's resource availability. Irrespective of access to resources, mothers, but not fathers, with many sons suffered from reduced post-reproductive survival, and this association decreased as mothers aged. Our results provide evidence that Finnish mothers traded long post-reproductive lifespan for giving birth to many sons.

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Accelerated immunosenescence in preindustrial twin mothers

Cited by 43 publications

References 45 publications

Differential fitness costs of reproduction between the sexes

Differential fitness costs of reproduction between the sexes

Early-life disease exposure and associations with adult survival, cause of death, and reproductive success in preindustrial humans

A trade-off between having many sons and shorter maternal post-reproductive survival in pre-industrial Finland

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