Survival costs and benefits of reproduction: A register-based study in 20th century Estonia.

Patterns of individual variation in lifespan and senescence depend on the associations between parental survival and reproductive rates. We studied the associations between parity and survival among 579,271 Estonians born between 1905 and 1945 and in a cohort with a completed lifespan born in 1905-1927. For this cohort, selection for increased lifespan operated on both sexes, but it was stronger in men than in women. However, the median lifespan increased between the subsequent cohorts in women but stagnated in men. Selection for longer lifespan was caused by the below-average lifespan of individuals with no or single offspring. Despite a general positive selection for lifespan, survival costs of reproduction were also detected among a relatively small proportion of individuals with high parities, as mothers of two and fathers of two and three children had the highest median lifespans. Fathers of more than six children had better survival than fathers of few children in their reproductive age, but this association reversed after age 70. The reversal of this association between survival and parity at old age indicates that relative mortality risks between those with lower versus higher parities change across ages, as predicted by the antagonistic pleiotropy theory of aging.

Mothers of small-bodied children and fathers of vigorous sons live longer.

Life-history traits (traits directly related to survival and reproduction) co-evolve and materialize through physiology and behavior. Accordingly, lifespan can be hypothesized as a potentially informative marker of life-history speed that subsumes the impact of diverse morphometric and behavioral traits. We examined associations between parental longevity and various anthropometric traits in a sample of 4,000-11,000 Estonian children in the middle of the 20th century. The offspring phenotype was used as a proxy measure of parental genotype, so that covariation between offspring traits and parental longevity (defined as belonging to the 90th percentile of lifespan) could be used to characterize the aggregation between longevity and anthropometric traits. We predicted that larger linear dimensions of offspring associate with increased parental longevity and that testosterone-dependent traits associate with reduced paternal longevity. Twelve of 16 offspring traits were associated with mothers' longevity, while three traits (rate of sexual maturation of daughters and grip strength and lung capacity of sons) robustly predicted fathers' longevity. Contrary to predictions, mothers of children with small bodily dimensions lived longer, and paternal longevity was not linearly associated with their children's body size (or testosterone-related traits). Our study thus failed to find evidence that high somatic investment into brain and body growth clusters with a long lifespan across generations, and/or that such associations can be detected on the basis of inter-generational phenotypic correlations.

Sexually antagonistic selection on educational attainment and body size in Estonian children.

Natural selection is a key mechanism of evolution, which results from the differential reproduction of phenotypes. We describe fecundity selection at different parity transitions on 15 anthropometric traits and educational attainment in Estonian children sampled in the middle of 20th century. The direction of selection on educational attainment and bodily traits was sexually antagonistic, and it occurred via different parity transitions in boys and girls. Compared to boys with primary education, obtaining tertiary education was associated with 3.5 times and secondary education two times higher odds of becoming a father. Transition to motherhood was not related to educational attainment, while education above primary was associated with lower odds (OR = 0.5-0.7) to progression to parities above one and two. Selection on anthropometric traits occurred almost exclusively via childlessness in boys, while among the girls, most of the traits that were associated with becoming a mother were additionally associated with a transition from one child to higher parities. Male (but not female) fitness was thus primarily determined by traits related to mating success. Selection favored stronger and larger boys and smaller girls. Selection on girls favored some traits that associate with perceived femininity, while other feminine traits were selected against.

Parental age does not influence offspring telomeres during early life in common gulls (Larus canus).

Parental age can affect offspring telomere length through heritable and epigenetic-like effects, but at what stage during development these effects are established is not well known. To address this, we conducted a cross-fostering experiment in common gulls (Larus canus) that enabled us distinguish between pre- and post-natal parental age effects on offspring telomere length. Whole clutches were exchanged after clutch completion within and between parental age classes (young and old) and blood samples were collected from chicks at hatching and during the fastest growth phase (11 days later) to measure telomeres. Neither the ages of the natal nor the foster parents predicted the telomere length or the change in telomere lengths of their chicks. Telomere length (TL) was repeatable within chicks, but increased across development (repeatability = 0.55, intraclass correlation coefficient within sampling events 0.934). Telomere length and the change in telomere length were not predicted by post-natal growth rate. Taken together, these findings suggest that in common gulls, telomere length during early life is not influenced by parental age or growth rate, which may indicate that protective mechanisms buffer telomeres from external conditions during development in this relatively long-lived species.

Anthropometrics of Estonian children in relation to family disruption: Thrifty phenotype and Trivers-Willard effects.

BACKGROUND AND OBJECTIVES: The thrifty phenotype hypothesis proposes that at resource limitation, the growth of some organs/tissues is selectively spared to preserve more critical ones, such as the brain or lungs. The Trivers-Willard hypothesis (TWH) predicts that boys are more vulnerable in the case of resource limitation than girls. Both hypotheses were tested in children from disrupted families, differing in the extent of deprivation/adversities imposed on them. METHODOLOGY: In a retrospective cohort study in the mid-20th century Estonia (Juhan Aul's database), different types of orphans and children of divorced parents (treatment groups; n = 106-1401) were compared with children from bi-parental families (control groups; n = 2548-8648) so that children from treatment groups were matched with control children on the basis of sex, age, year of birth, urban versus rural origin and socioeconomic position. RESULTS: Children in orphanages suffered strong growth suppression, best explained by psychosocial deprivation. Their feet were on average 0.5 SD shorter than the feet of the controls, followed by height, leg/torso ratio and cranial volume that differed from controls by ca 0.4 SD. Weight difference was 0.2 SD units, while body mass index did not differ from controls. The growth of boys and girls in orphanages was suppressed to the same extent. Boys whose mothers were dead were relatively smaller and less masculine than girls from such families. Fathers' absence was unrelated to growth suppression. Sons of divorced parents had broader shoulders than boys whose fathers were dead. CONCLUSIONS AND IMPLICATIONS: Prediction of TWH about the greater vulnerability of male growth may hold under some conditions but not universally. Predictions of the thrifty phenotype hypothesis were partly supported: trunk growth was spared at the expense of leg growth; however, no evidence for brain sparing was found. Comparison of children of divorced versus dead fathers may appear useful for indirect assessment of sexual selection on offspring quality.Lay Summary: Boys and girls in orphanages suffered similarly strong growth suppression, best explained by psychosocial deprivation. Boys whose mothers were dead were relatively smaller and less masculine than girls from such families. The occurrence of sex-specific associations between family structure and children's growth depends on the type of family disruption.

Antibiotic treatment increases yellowness of carotenoid feather coloration in male greenfinches (Chloris chloris).

Carotenoid plumage coloration is an important sexually selected trait in many bird species. However, the mechanisms ensuring the honesty of signals based on carotenoid pigments remain unclear. It has recently been suggested that intestinal integrity, which is affected by gut parasites and microbiota and influences nutrient absorption and acquisition, mediates the relationship between carotenoid ornamentation and individual quality. Here, we test whether carotenoid plumage coloration in greenfinches (Chloris chloris) is affected by the treatment of an antibiotic or an antiparasitic drug. We captured wild greenfinches (N = 71) and administered anticoccidial medication toltrazuril (TOLTRA) to one group, antibiotic metronidazole (METRO) to the second group to target trichomonosis, and the third group received no medication. In the METRO group, feathers grown during the experiment had significantly higher chroma of yellow parts, but there was no effect of TOLTRA on feather chroma. The results suggest that METRO increased the efficiency of carotenoid modification or deposition to the feathers rather than nutrient acquisition and/or freed energy resources that could be invested in coloration. Alternatively, though not measured, METRO might have affected microbial community and host physiology as microbial metabolites can modulate mitochondrial and immune function.

Adolescent Cranial Volume as a Sensitive Marker of Parental Investment: The Role of Non-material Resources?

Growth of different body parts in humans is sensitive to different resource constraints that are mediated by parental investment. Parental investment can involve the expenditure of material, cognitive, and emotional resources on offspring. Cranial volume, an important predictor of cognitive ability, appears understudied in this context. We asked (1) whether there are associations between growth and family structure, self-reported estimates for resource availability, and sibling number; and (2) whether these constraints relate to head and body growth in a similar manner. We assessed the associations between parental investment, height, and cranial volume in a cross-sectional study of Estonian children (born 1980-87, aged 11-17). Height correlated negatively with the number of siblings but this association became negligible in a model controlling for birthweight, parental heights, and mother's age at birth. Unlike height, cranial volume was unrelated to sibling number, but it was negatively associated with self-reported meat and general resource shortage. Cranial volume was related to family structure and paternal education. Children living with both birth-parents had larger heads than those living in families containing a step-parent. Since these family types did not differ with respect to meat or general resource shortage, our findings suggest that families including both genetic parents provide non-material benefits that stimulate predominantly cranial growth. For the studied developmental period, cranial volume appeared a more sensitive marker of growth constraints than height. The potential of using cranial volume for quantifying physical impact of non-material parental investment deserves further attention.

Corticosterone levels correlate in wild-grown and lab-grown feathers in greenfinches (Carduelis chloris) and predict behaviour and survival in captivity.

Level of corticosterone (CORT), which is a predominant glucocorticoid in birds, has become the main indicator for assessing the stress level of birds in ecological studies. Feather corticosterone (CORTf) provides information about corticosterone levels during feather growth, however, the underlying causes of individual variation of CORTf between individuals and individual persistency of CORTf are not yet fully understood. Therefore, this study addresses individual consistency in CORTf and the association of variation in CORTf with behaviour that results in damage to tail feathers. We studied relations between CORTf, plasma CORT, and behaviour in wild-caught male greenfinches in captivity. CORTf in wild-grown feathers correlated positively with CORTf in lab-grown feathers. CORTf levels were about 20% lower in lab-grown feathers than in those grown in the wild. Four birds that died in captivity had significantly higher average CORTf levels in wild-grown feathers than the survivors. Plasma CORT levels of two measurements taken in the lab seven days apart correlated positively, however, no correlations between plasma CORT and CORTf were found. In order to study the link between CORTf and behaviour, the extent of tail damage from flapping against cage bar was assessed. Contrary to our prediction, birds with higher CORTf had less tail damage. This study adds to the evidence that CORTf levels can be considered as informative markers of some persistent component of individual phenotypic quality that can predict survival under standardized laboratory conditions.

Morphometric traits predict educational attainment independently of socioeconomic background.

BACKGROUND: Aim of this study is to describe the relationship between anthropometric traits and educational attainment among Estonian schoolchildren born between 1937 and 1962. We asked whether height, cranial volume and face width (a testosterone-dependent trait), measured in childhood predict later educational attainment independently of each other, family socioeconomic position (SEP) and sex. Associations between morphometric traits and education and their interactions with biosocial variables are of scholarly importance because higher education is nearly universally associated with low fertility in women, and often with high fertility in men. Hence, morphometric traits associated with educational attainment are targeted by natural selection and describing the exact nature of these associations is relevant for understanding the current patterns of evolution of human body size. METHODS: Data on morphometric measurements and family background of 11,032 Estonian schoolchildren measured between seven and 19 years of age were obtained from the study performed by Juhan Aul between 1956 and 1969. Ordinal logistic regression was used for testing the effects of morphometric traits, biosocial variables and their interaction on the cumulative probability of obtaining education beyond primary level. RESULTS: Of biosocial variables, family SEP was the most important determinant of educational attainment, followed by the sex, rural vs urban origin and the number of siblings. No significant interactions with morphometric traits were detected, i.e., within each category of SEP, rural vs urban origin and sex, taller children and those with larger heads and relatively narrower faces were more likely to proceed to secondary and/or tertiary education. The effect of height on education was independent of cranial volume, indicating that taller children did not obtain more educations because their brains were larger than those of shorter children; height per se was important. CONCLUSIONS: Our main finding - that adjusting for other morphometric traits and biosocial variables, morphometric traits still robustly predicted educational attainment, is relevant for understanding the current patterns of evolution of human body size. Our findings suggest that fecundity selection acting on educational attainment could be partly responsible for the concurrent selection for smaller stature and cranial volume in women and opposite trends in men.

Parents of early-maturing girls die younger.

According to the life-history theory, rates of sexual maturation have coevolved with mortality rates so that individuals who mature faster tend to die younger. We used two data sets, providing different markers for the speed of pubertal development to test whether rates of sexual maturation of women predict the age at death of their parents. In the data set of Estonian schoolgirls born between 1936 and 1961, the rate of breast development predicted lifespan of both mothers and fathers (irrespectively of their socio-economic position), so that parents of rapidly maturing girls died at younger age. This finding supports the view that fast maturation rates in humans have coevolved with short lifespans and that such trade-offs can be detected as intergenerational phenotypic correlations in modern populations. Menarcheal age of participants of Estonian Biobank (born between 1925 and 1996) did not predict the age of death of their mothers; however, it did predict survival of their fathers, but only in environment where the genetic variation is exposed (families where at least one parent had tertiary education). In such families (where girls also matured 0.2-0.4 years earlier than in poorly educated families), 1-year delay in daughter's menarche corresponded to 9% lower hazard of father's death. Heritability of menarcheal age was also highest in well-educated families. The latter findings are consistent with the idea that genetic differences in the rate of pubertal maturation may be expressed most clearly in well-off families because in such families, the contribution of environmental variance to total phenotypic variance in menarcheal age is smallest. Our findings suggest that with global improvement and equalization of growth conditions, reductions of environmental variation in the rate of maturation increasingly expose the genetic differences in menarcheal age to selection. Under such conditions, selection on menarcheal age has a potential to affect the evolution of lifespan.

Uropygial gland size: a marker of phenotypic quality that shows no senescence in a long-lived seabird.

Studies of senescence in the wild have traditionally focused on traits like survival or fecundity. Although efforts to measure other salient phenotypic traits and markers of relevant physiological processes are rapidly increasing, traits related to self-maintenance remain understudied in the context of aging. Uropygial or preen gland is a holocrine gland, exclusive to birds, directly linked to self-maintenance of the quality of plumage. We measured the size of uropygial glands of common gulls (Larus canus) in a cross sectional manner in order to test whether it shows the similar age-related decline as reproductive traits previously recorded in this species. Gulls with larger glands started breeding earlier in the season, indicating that gland size is a marker of individual phenotypic quality. We found a senescent decline in the onset of breeding and the size of white wing patches, a sexually dimorphic ornamental trait, while in contrast, preen gland increased with advancing age. This finding supports the view of life-history theory that in long-lived species whose lifetime reproductive success depends heavily on lifespan, self-maintenance is prioritized over reproduction. Altogether our results support the concept that senescence in the wild can be asynchronous for traits related to maintenance versus reproduction.

Demographic and evolutionary trends in ovarian function and aging.

BACKGROUND: The human female reproductive lifespan is regulated by the dynamics of ovarian function, which in turn is influenced by several factors: from the basic molecular biological mechanisms governing folliculogenesis, to environmental and lifestyle factors affecting the ovarian reserve between conception and menopause. From a broader point of view, global and regional demographic trends play an additional important role in shaping the female reproductive lifespan, and finally, influences on an evolutionary scale have led to the reproductive senescence that precedes somatic senescence in humans. OBJECTIVE AND RATIONALE: The narrative review covers reproductive medicine, by integrating the molecular mechanisms of ovarian function and aging with short-term demographic and long-term evolutionary trends. SEARCH METHODS: PubMed and Google Scholar searches were performed with relevant keywords (menopause, folliculogenesis, reproductive aging, reproductive lifespan and life history theory). The reviewed articles and their references were restricted to those written in English. OUTCOMES: We discuss and summarize the rapidly accumulating information from large-scale population-based and single-reproductive-cell genomic studies, their constraints and advantages in the context of female reproductive aging as well as their possible evolutionary significance on the life history trajectory from foetal-stage folliculogenesis until cessation of ovarian function in menopause. The relevant environmental and lifestyle factors and demographic trends are also discussed in the framework of predominant evolutionary hypotheses explaining the origin and maintenance of menopause. WIDER IMPLICATIONS: The high speed at which new data are generated has so far raised more questions than it has provided solid answers and has been paralleled by a lack of satisfactory interpretations of the findings in the context of human life history theory. Therefore, the recent flood of data could offer an unprecedented tool for future research to possibly confirm or rewrite human evolutionary reproductive history, at the same time providing novel grounds for patient counselling and family planning strategies.

Age-specific patterns of maternal investment in common gull egg yolk.

While the general patterns of age-specific changes in reproductive success are quite well established in long-lived animals, we still do not know if allocation patterns of maternally transmitted compounds are related to maternal age. We measured the levels of yolk testosterone, carotenoids and vitamins A and E in a population of known-aged common gulls (Larus canus) and found an age-specific pattern in yolk lutein and vitamin A concentrations. Middle-aged mothers allocated more of these substances to yolk compared to young and old mothers. These results can be explained through differences in age-specific foraging, absorption or deposition patterns of carotenoids and vitamins into yolk. If these molecules play a role in antioxidant defence and immune modulation, our results suggest a possible physiological pathway underlying the age-specific changes in reproductive success of long-lived birds in the wild.

Simple and noninvasive method for assessment of digestive efficiency: Validation of fecal steatocrit in greenfinch coccidiosis model.

Animals' capability to absorb energy and nutrients from food poses a major internal constraint that affects the amount of resources available for allocation to maintenance, growth, signaling, and reproduction. Intestinal surface is the largest area of contact between immune system and microbial antigens; gut thus appears the main arena where trade-offs between immune function and other components of fitness arise. Assessment of the integrity of digestive machinery should therefore be of high priority in ecophysiological research. Traditional methods of digestive physiology, however, appear unsuitable for most ecological applications due to lethality or complexity of the procedure.Here, we test the reliability of a simple, cheap, and noninvasive procedure, an acid steatocrit that assesses fat content in feces. It is based on centrifugation of a fecal sample, diluted in acid medium, in hematocrit capillary tube and quantifying the percentage of fat in fecal matter. The method has been previously validated in humans and mice; here, we apply it for the first time in birds.When applied to captive wild-caught greenfinches, the method showed reasonable internal consistency (rs = 0.71 for steatocrit values, sampled from the same fecal aliquot in duplicate but processed separately). Individual steatocrit values were significantly repeatable in time in different intervals from eight to at least 20 days (rs = 0.32-0.49). The relationship between intestinal health and steatocrit values was tested by experimental manipulations. Medication against coccidiosis (a naturally pervasive intestinal infection) reduced, and experimental infection with heterologous coccidian strains increased steatocrit. Individual changes in steatocrit correlated negatively with changes of two markers of nutritional state-plasma triglyceride levels and body mass.Findings of this study suggest that steatocrit has a wide application potential as a marker of intestinal health in ecophysiological research. In particular, we see the perspective of this method for increasingly popular immunoecological research, conservation medicine, and studies of animal coloration.

Variation in the Markers of Nutritional and Oxidative State in a Long-Lived Seabird: Associations with Age and Longevity.

Age-related declines in life-history traits have been widely observed in free-living animals. Several theories link senescence to oxidative stress. The aim of this study was to measure several widely used markers of oxidative and nutritional state in a long-lived seabird, the common gull (Larus canus), in order to assess the suitability of these markers for describing deterioration in physiological condition associated with chronological age and survival. Associations with longevity and individual consistency of these parameters over the years (repeatability) were also assessed. Senescence in fitness parameters was observed during the study period: in females, laying date and clutch mass were related to bird age in a curvilinear manner, with middle-aged birds breeding earlier and laying heavier eggs. The only parameter associated with aging processes was glutathione concentration in erythrocytes, which was lower in female birds with longer life spans. Of indexes of nutritional state, plasma triglyceride concentration showed a between-individual increase with age, suggesting selective mortality of birds with low levels. Additionally, total plasma protein levels of individual males increased with age. The mostly negative results of this study hint that the commonly used parameters of physiological condition and oxidative state used in this study do not adequately reflect an individual's long-term health condition. Alternatively, it is possible that in common gulls, senescence occurs in reproductive mechanisms but not in mechanisms responsible for maintaining an organism's redox balance, consistent with the idea that different aspects of an organism's physiological condition age at different rates. Significant interannual repeatability was detected in three plasma constituents-carotenoids, uric acid, and total protein-all of which can possibly be linked to variation in dietary habits.

Viability selection affects black but not yellow plumage colour in greenfinches.

Much of the debate surrounding the selective forces responsible for the expression of conspicuous plumage colouration is centred on the question of precisely which individual qualities are signalled by carotenoid- and melanin-based pigments. To examine this and other related issues, we performed viability selection analyses in wild-caught captive male greenfinches (Carduelis chloris) in Estonia during winters between 2003 and 2014. Based on our measurements, birds with a darker black eumelanin-based colouration of tail feathers survived better than those whose tail feathers had a paler black colouration. The carotenoid-based yellow colouration of the same feathers was not associated with mortality in captivity and showed much less between-year variation in the field than the black colouration. Between year-variation in the black (but not yellow) colouration of feathers was parallel in wild-grown feathers (on birds in the wild) and laboratory-grown ones (on birds held temporarily in captivity). Taken together, these findings imply that eumelanotic colouration in greenfinches is currently under selection and suggest the presence of sufficient genetic variation for a rapid response to selection. In particular, tail feathers have become darker black since the emergence of avian trichomonosis, which is known to selectively kill paler individuals.

Father's death does not affect growth and maturation but hinders reproduction: evidence from adolescent girls in post-war Estonia.

The popular concept of predictive-adaptive responses poses that girls growing up without a father present in the family mature and start reproduction earlier because the father's absence is a cue for environmental harshness and uncertainty that favours switching to a precocious life-history strategy. Most studies supporting this concept have been performed in situations where the father's absence is caused by divorce or abandonment. Using a dataset of Estonian adolescent girls who had lost their fathers over the period of World War II, we show that father's death did not affect the rate of pubertal maturation (assessed on the basis of development of breasts and axillary hair) or growth. Father's death did not affect the age of first birth but, contrary to predictions, reduced lifetime reproductive success. Our findings thus do not support the concept of predictive-adaptive responses and suggest that alternative explanations for covariation between fatherlessness and early maturation are required.

Why did children grow so well at hard times? The ultimate importance of pathogen control during puberty.

BACKGROUND AND OBJECTIVES: Secular increase in human height and performance occurred in Europe throughout the 20th century despite the temporally worsening access to nutrients during and after World War II. This pattern is paradoxical under the assumption of the major impact of pre- and postnatal growth conditions for determination of adult size and human capital. METHODOLOGY: We examined the anthropometric parameters of Estonian girls born between 1938 and 1953, and measured around the age of 17 (n = 1475). This period involved two opposite trends in the economic and epidemiological situation: increasing birth-time economic hardships during the war and particularly in the post-war period, and decreasing infant mortality (a proxy of disease burden) after 1947. RESULTS: Height of girls was negatively affected by the number of siblings and positively by parental socioeconomic position, but these effects were weaker than the secular trend. Leg length (an indicator of pre-pubertal growth conditions) was independent of age and birth date while all other traits, including measures of performance (cranial volume, lung capacity and handgrip strength) showed acceleration. The best predictor of size at age 17 was, in most cases, infant mortality in the year when the girls were aged 11. CONCLUSIONS AND IMPLICATIONS: Reduction of disease burden during pubertal growth can override effects of resource shortage at birth. Our results also support the idea that increasing efficiency of pathogen control can contribute to the secular increase in cognitive abilities, i.e. the Flynn effect, and that epidemiological transition is the main driver of secular increase in human capital.

Skin pentosidine and telomere length do not covary with age in a long-lived seabird.

The questions about why and how senescence occurs in the wild are among the most pertinent ones in evolutionary ecology. Telomere length is a commonly used marker for aging, while other biomarkers of aging have received considerably less attention. Here we studied how another potent indicator of aging-skin pentosidine concentration-relates to age and blood telomere length in a long-lived seabird with well-documented reproductive senescence. We found no associations between telomere length, skin pentosidine and chronological age in male common gulls (Larus canus), aging from 2 to 30 years. However, the variance in telomere length was 4.6 times higher among the birds older than 13 years, which hints at relaxed selection on telomere length among the birds that have passed their prime age of reproduction. These results suggest that physiological and chronological ages may be largely uncoupled in our study system. Furthermore, our findings do not support a hypothesis about the presence of a common physiological factor (e.g., such as oxidative stress) that would cause covariation between two independent markers of aging.