Variation in testosterone levels and male reproductive effort: Insight from a polygynous human population

Recent evidence suggests that, in humans, variations in testosterone (T) levels between men reflect their differential allocation in mating versus parenting efforts. However, most studies have been conducted in urbanized, monogamous populations, making generalizations from them questionable. This study addresses the question of whether indicators of male reproductive effort are associated with variations in salivary T levels in a polygynous population of agriculturists in rural Senegal. We first show that pair-bonding and/or transition to fatherhood is associated with T profiles: married fathers (N = 53) have lower morning and afternoon T levels than unmarried non-fathers (N = 28). Second, among fathers, individual differences in parenting effort, as well as variations in mating effort, predict morning T levels. Indeed, men highly investing in parental care show lower morning T levels. Moreover, among men under 50, polygynous men show higher morning T levels than monogamous men. Taken together with previous results in monogamous settings, these findings suggest that the endocrine regulation of reproductive effort is probably a general feature of human populations.     

Variation in testosterone levels and male reproductive effort: Insight from a polygynous human population

Recent evidence suggests that, in humans, variations in testosterone (T) levels between men reflect their differential allocation in mating versus parenting efforts. However, most studies have been conducted in urbanized, monogamous populations, making generalizations from them questionable. This study addresses the question of whether indicators of male reproductive effort are associated with variations in salivary T levels in a polygynous population of agriculturists in rural Senegal. We first show that pair-bonding and/or transition to fatherhood is associated with T profiles: married fathers (N = 53) have lower morning and afternoon T levels than unmarried non-fathers (N = 28). Second, among fathers, individual differences in parenting effort, as well as variations in mating effort, predict morning T levels. Indeed, men highly investing in parental care show lower morning T levels. Moreover, among men under 50, polygynous men show higher morning T levels than monogamous men. Taken together with previous results in monogamous settings, these findings suggest that the endocrine regulation of reproductive effort is probably a general feature of human populations.     

Testosterone levels correlate with the number of children in human males,but the direction of the relationship depends on paternal education

Most research shows that fatherhood is related to reduced testosterone (T) levels, but relationships between the number of children and T levels are not addressed. In humans, paternal care usually involves obtaining adequate resources to support children, which may require engaging in male–male competition and maintaining high T levels. We hypothesize that T levels in fathers should increase with increasing family size. In 78 Polish men, aged 30 to 77 years, the number of children was significantly correlated with paternal T levels, but the direction of this relationship was dependent on the fathers' education. In agreement with our hypothesis, in men with below-college education, T levels increased with increasing number of children. In contrast, in men with college education, the number of children was negatively related to paternal T levels. Drop in T levels throughout the day tended to be less pronounced the more children fathers had, irrespective of their educational level. Our results suggest that a hypothesis of simple trade-offs between mating and parenting effort may be too simplistic to explain changes in testosterone response to parenting in human males. In order to understand functional response of changes in T levels, it is crucial to account for family size and socioeconomic factors. However, due to the cross-sectional study design, we cannot exclude the possibility that T levels influenced reproductive behavior (rather than vice versa) and thus the number of children produced by men.     

Marriage and fatherhood are associated with lower testosterone in males

In order to study the hormonal correlates of the tradeoff between mating and parenting effort in human males, we examined the salivary testosterone (T) levels of 58 Boston-area men who were either unmarried (n=29), married without children (n=14), or married with children (n=15). Additionally, we asked participants to complete a questionnaire that surveyed their demographic, marital, and parenting backgrounds. We tested the hypotheses that (1) T levels will be lower in married than in unmarried men and (2) married men with children will have lower T levels than unmarried men and married men without children. We also tested a series of hypotheses relating variation in parenting and spousal relationships to T. We found that married men with and without children had significantly lower evening T than unmarried men. No significant differences in T were found among the groups in morning samples. Among married men without children, higher scores on a “spousal investment” measure and more hours spent with a man's wife on his last day off work were both associated with lower T levels. We suggest that lower T levels during the day among fathers may facilitate paternal care in humans by decreasing the likelihood that a father will engage in competitive and/or mating behavior.     

Marriage, parenting, and testosterone variation among Kenyan Swahili men

Male variation in testosterone (T) levels may, in part, reflect a differential behavioral allocation to mating and parenting effort. This research tests whether demographic indicators of pair bonding and parenting were associated with salivary T levels among Kenyan Swahili men. Men in the sample were either unmarried (N = 17), monogamously married (N = 57), or polygynously married (N = 14), and between ages 29-52. In contrast with earlier findings among North American men, monogamously married men did not have lower T levels than unmarried men. However, among all married men, men with younger genetic children tended to have marginally lower T levels. Polygynously married men, all of whom had two wives, had higher T levels than all other Swahili men. Possible explanations of higher T levels among polygynously married men are explored.     

Testosterone and paternal care in East African foragers and pastoralists

The 'challenge hypothesis' posits that testosterone facilitates reproductive effort (investment in male-male competition and mate-seeking) at the expense of parenting effort (investment in offspring and mates). Multiple studies, primarily in North America, have shown that men in committed relationships, fathers, or both maintain lower levels of testosterone than unpaired men. Data from non-western populations, however, show inconsistent results. We hypothesized that much of this cross-cultural variation can be attributed to differential investment in mating versus parenting effort, even among married fathers. Here, we directly test this idea by comparing two neighbouring Tanzanian groups that exhibit divergent styles of paternal involvement: Hadza foragers and Datoga pastoralists. We predicted that high levels of paternal care by Hadza fathers would be associated with decreased testosterone in comparison with non-fathers, and that no such difference between fathers and non-fathers would be evident in Datoga men, who provide minimal direct paternal care. Twenty-seven Hadza men and 80 Datoga men between the ages of 17 and 60 provided morning and afternoon saliva samples from which testosterone was assayed. Measurements in both populations confirmed these predictions, adding further support to the hypothesis that paternal care is associated with decreased testosterone production in men.     

Fathers have lower salivary testosterone levels than unmarried men and married non-fathers in Beijing, China

A growing body of evidence, almost entirely from North America, has found that male testosterone levels are positively associated with mating effort (male-male competition and mate-seeking behaviour), while lower testosterone levels have been associated with affiliative pair bonding and paternal care. To expand the cross-cultural scope of this research, here we investigate variation in salivary testosterone levels among Chinese men in relation to marital and parenting variables. One hundred and twenty-six men drawn from a Beijing university setting between the ages of 21 and 38 completed a questionnaire and provided both morning and late afternoon saliva samples from which testosterone levels were measured. The 66 unmarried men had slightly higher levels of testosterone than the 30 married non-fathers, but this difference was not statistically significant. However, the 30 fathers exhibited significantly lower testosterone levels than both unmarried men and married non-fathers. Among married non-fathers, marital relationship quality was not significantly related to testosterone levels. Among married fathers, men with children aged less than 4 years of age did not have lower testosterone levels than men with older children. These data are the first outside of North America to show lower testosterone levels among fathers, and lend support to the theoretical view that male testosterone levels differ according to mating and parenting effort.     

Does Cosleeping Contribute to Lower Testosterone Levels in Fathers? Evidence from the Philippines

Because cross-species evidence suggests that high testosterone (T) may interfere with paternal investment, the relationships between men''s transition to parenting and changes in their T are of growing interest. Studies of human males suggest that fathers who provide childcare often have lower T than uninvolved fathers, but no studies to date have evaluated how nighttime sleep proximity between fathers and their offspring may affect T. Using data collected in 2005 and 2009 from a sample of men (n = 362; age 26.0 ± 0.3 years in 2009) residing in metropolitan Cebu, Philippines, we evaluated fathers'' T based on whether they slept on the same surface as their children (same surface cosleepers), slept on a different surface but in the same room (roomsharers), or slept separately from their children (solitary sleepers). A large majority (92%) of fathers in this sample reported practicing same surface cosleeping. Compared to fathers who slept solitarily, same surface cosleeping fathers had significantly lower evening (PM) T and also showed a greater diurnal decline in T from waking to evening (both p<0.05). Among men who were not fathers at baseline (2005), fathers who were cosleepers at follow-up (2009) experienced a significantly greater longitudinal decline in PM T over the 4.5-year study period (p<0.01) compared to solitary sleeping fathers. Among these same men, baseline T did not predict fathers'' sleeping arrangements at follow-up (p>0.2). These results are consistent with previous findings indicating that daytime father-child interaction contributes to lower T among fathers. Our findings specifically suggest that close sleep proximity between fathers and their offspring results in greater longitudinal decreases in T as men transition to fatherhood and lower PM T overall compared to solitary sleeping fathers.     

Modernization,Sexual Risk-Taking,and Gynecological Morbidity among Bolivian Forager-Horticulturalists

Sexual risk-taking and reproductive morbidity are common among rapidly modernizing populations with little material wealth, limited schooling, minimal access to modern contraception and healthcare, and gendered inequalities in resource access that limit female autonomy in cohabiting relationships. Few studies have examined how modernization influences sexual risk-taking and reproductive health early in demographic transition. Tsimane are a natural fertility population of Bolivian forager-farmers; they are not urbanized, reside in small-scale villages, and lack public health infrastructure. We test whether modernization is associated with greater sexual risk-taking, report prevalence of gynecological morbidity (GM), and test whether modernization, sexual risk-taking and parity are associated with greater risk of GM. Data were collected from 2002–2010 using interviews, clinical exams, and laboratory analysis of cervical cells. We find opposing effects of modernization on both sexual risk-taking and risk of GM. Residential proximity to town and Spanish fluency are associated with greater likelihood of men’s infidelity, and with number of lifetime sexual partners for men and women. However, for women, literacy is associated with delayed sexual debut after controlling for town proximity. Fifty-five percent of women present at least one clinical indicator of GM (n = 377); 48% present inflammation of cervical cells, and in 11% the inflammation results from sexually transmitted infection (trichomoniasis). Despite having easier access to modern healthcare, women residing near town experience greater likelihood of cervical inflammation and trichomoniasis relative to women in remote villages; women who are fluent in Spanish are also more likely to present trichomoniasis relative to women with moderate or no fluency. However, literate women experience lower likelihood of trichomoniasis. Parity has no effect on risk of GM. Our results suggest a net increase in risk of reproductive morbidity among rapidly modernizing, resource-stressed populations.     

An ACACB Variant Implicated in Diabetic Nephropathy Associates with Body Mass Index and Gene Expression in Obese Subjects

Acetyl coenzyme A carboxylase B gene (ACACB) single nucleotide polymorphism (SNP) rs2268388 is reproducibly associated with type 2 diabetes (T2DM)-associated nephropathy (DN). ACACB knock-out mice are also protected from obesity. This study assessed relationships between rs2268388, body mass index (BMI) and gene expression in multiple populations, with and without T2DM. Among subjects without T2DM, rs2268388 DN risk allele (T) associated with higher BMI in Pima Indian children (n = 2021; p-additive = 0.029) and African Americans (AAs) (n = 177; p-additive = 0.05), with a trend in European Americans (EAs) (n = 512; p-additive = 0.09), but not Germans (n = 858; p-additive = 0.765). Association with BMI was seen in a meta-analysis including all non-T2DM subjects (n = 3568; p-additive = 0.02). Among subjects with T2DM, rs2268388 was not associated with BMI in Japanese (n = 2912) or EAs (n = 1149); however, the T allele associated with higher BMI in the subset with BMI≥30 kg/m² (n = 568 EAs; p-additive = 0.049, n = 196 Japanese; p-additive = 0.049). Association with BMI was strengthened in a T2DM meta-analysis that included an additional 756 AAs (p-additive = 0.080) and 48 Hong Kong Chinese (p-additive = 0.81) with BMI≥30 kg/m² (n = 1575; p-additive = 0.0033). The effect of rs2268388 on gene expression revealed that the T risk allele associated with higher ACACB messenger levels in adipose tissue (41 EAs and 20 AAs with BMI>30 kg/m²; p-additive = 0.018) and ACACB protein levels in the liver tissue (mixed model p-additive = 0.03, in 25 EA bariatric surgery patients with BMI>30 kg/m² for 75 exams). The T allele also associated with higher hepatic triglyceride levels. These data support a role for ACACB in obesity and potential roles for altered lipid metabolism in susceptibility to DN.     

American legacies and the variable life histories of women and men

Sex differences in behavior are most interesting when they are the result of inherent differences in the operational rules motivating behavior and not merely a reflection of differing life history experiences. American men and women exhibit a few differences in testamentary patterns of property allocation that appear to be due to inherently different rules of allocation. Even when analyses control for resources and surviving kin configurations, women distribute their property among a greater number of individual beneficiaries than do men. The most striking differences in property allocation between men and women occur within the nuclear family and reflect differences in reproductive life span and the resulting reproductive conflicts between spouses that can endure beyond death. The initial research for this paper was funded by a grant to Sarah Blaffer Hrdy and the author from the Rockefeller Foundation Program in Changing Gender Roles. Debra Judge is associated with the Ecology Graduate Group and the Department of Anthropology at the University of California at Davis. Her interests focus on human demography, reproductive strategies, and the ecological conditions influencing human mating and parenting strategies—especially intergenerational resource transfer.     

Do testosterone declines during the transition to marriage and fatherhood relate to men's sexual behavior? Evidence from the Philippines

Testosterone (T) is thought to help facilitate trade-offs between mating and parenting in humans. Across diverse cultural settings married men and fathers have lower T than other men and couples' sexual activity often declines during the first years of marriage and after having children. It is unknown whether these behavioral and hormonal changes are related. Here we use longitudinal data from a large study in the Philippines (n = 433) to test this model. We show that among unmarried non-fathers at baseline (n = 153; age: 21.5 ± 0.3 years) who became newly married new fathers by follow-up (4.5 years later), those who experienced less pronounced longitudinal declines in T reported more frequent intercourse with their partners at follow-up (p < 0.01) compared to men with larger declines in T. Controlling for duration of marriage, findings were similar for men transitioning from unmarried to married (without children) (p < 0.05). Men who remained unmarried and childless throughout the study period did not show similar T-sexual activity outcomes. Among newly married new fathers, subjects who had frequent intercourse both before and after the transition to married fatherhood had more modest declines in T compared to peers who had less frequent sex (p < 0.001). Our findings are generally consistent with theoretical expectations and cross-species empirical observations regarding the role of T in male life history trade-offs, particularly in species with bi-parental care, and add to evidence that T and sexual activity have bidirectional relationships in human males.     

Fertility Desires among Men and Women Living with HIV/AIDS in Nairobi Slums: A Mixed Methods Study

Objectives

Fertility desires require new understanding in a context of expanding access to antiretroviral therapy for people living with HIV/AIDS in Sub-Saharan Africa. This paper studies the fertility desires and their rationales, of slum-dwelling Kenyan men and women living with HIV/AIDS who know their serostatus, but have different antiretroviral therapy treatment statuses. It addresses two research questions: How do people living with HIV/AIDS consider their future fertility? What factors contribute to an explanation of fertility desires among people living with HIV/AIDS.

Methods

A mixed methods study (survey [n = 513] and in-depth interviews [n = 41]) with adults living with HIV/AIDS living in Nairobi slums was conducted in 2010. Regression analyses assess independent relationships between fertility desires and socio-demographic factors. Analyses of in-depth interviews are used to interpret the statistical analyses of fertility desires.

Results

Our analyses show that fertility desires are complex and ambivalent, reflecting tensions between familial and societal pressures to have children versus pressures for HIV (re-)infection prevention. More than a third (34%) of men and women living with HIV expressed future fertility desires; however, this is significantly lower than in the general population. Factors independently associated with desiring a child among people living with HIV/AIDS were age, sex, number of surviving children, social support and household wealth of the respondent.

Discussion

Increasing access to ART is changing the context of future childbearing for people living with HIV/AIDS. Prevailing values mean that, for many people living with HIV/AIDS, having children is seen as necessary for a “normal” and healthy adult life. However, the social rewards of childbearing conflict with moral imperatives of HIV prevention, presenting dilemmas about the “proper” reproductive behaviour of people living with HIV/AIDS. The health policy and service delivery implications of these findings are explored.     

Diurnal testosterone variability is differentially associated with parenting quality in mothers and fathers

Previous studies on the relation between testosterone (T) levels and parenting have found ample evidence for the challenge hypothesis, demonstrating that high T levels inhibit parental involvement and that becoming a parent is related to a decrease in T levels in both mothers and fathers. However, less is known about the relation between T levels and more qualitative aspects of parenting. In the current study we examined basal T levels and diurnal variability in T levels in relation to mothers' and fathers' parenting quality. Participants included 217 fathers and 124 mothers with two children (3 and 5 years of age). Evening and morning salivary T samples were analyzed with radio-immunoassays to determine circulating T levels. Parental sensitivity (i.e., child-centered responsiveness) and respect for children's autonomy were observed during free play in the family home. The results showed that higher evening T levels in mothers were associated with more sensitivity to the oldest and youngest child. Diurnal T variability was more consistently associated with parenting behavior towards their children than basal T levels. For fathers, more diurnal variability in T was associated with more sensitivity and more respect for autonomy with their youngest children. For mothers, more diurnal variability in T was associated with less sensitivity to both children and less respect for the youngest child's autonomy. These findings suggest that the T system might act differently in relation to parenting behavior in males and females.     

Testosterone levels and their associations with lifetime number of opposite sex partners and remarriage in a large sample of American elderly men and women

Testosterone (T) has been argued to modulate mating and parenting behavior in many species, including humans. The role of T for these behaviors has been framed as the challenge hypothesis. Following this hypothesis, T should be positively associated with the number of opposite sex partners a male has. Indeed research in humans has shown that T is positively related to the number of opposite sex partners a young man has had. Here we test, in both men and women, whether this relationship extends to the lifetime number of sex partners. We also explored whether or not T was associated with current marital status, partnership status and whether or not the participant remarried. Using a large sample of elderly men and women (each sample n > 700), we show that T is positively and sizably associated with the number of opposite sex partners in men. When controlling for potential confounding variables such as educational attainment, age, BMI, ethnicity, specific use of a medication and time of sampling this effect remained. For women, the relationship between T and number of opposite sex partners was positive but did not prove to be robust. In both men and women there was no evidence for an association between T and current marital status and partnership status (being in a relationship or not). However, remarriage was positively associated with T, but only in males. Results are discussed with reference to the literature on T and sex partners, remarriage and more broadly the challenge hypothesis.     

Association between Decreased Klotho Blood Levels and Organic Growth Hormone Deficiency in Children with Growth Impairment

Objective

Klotho is an aging-modulating protein expressed mainly in the kidneys and choroid plexus, which can also be shed, released into the circulation and act as a hormone. Klotho deficient mice are smaller compared to their wild-type counterparts and their somatotropes show marked atrophy and reduced number of secretory granules. Recent data also indicated an association between klotho levels and growth hormone (GH) levels in acromegaly. We aimed to study the association between klotho levels and GH deficiency (GHD) in children with growth impairment.

Design

Prospective study comprising 99 children and adolescents (aged 9.0±3.7 years, 49 male) undergoing GH stimulation tests for short stature (height-SDS = −2.1±0.6). Klotho serum levels were measured using an α-klotho ELISA kit.

Results

Klotho levels were significantly lower (p<0.001) among children with organic GHD (n = 11, 727±273 pg/ml) compared to both GH sufficient participants (n = 59, 1497±754 pg/ml) and those with idiopathic GHD (n = 29, 1645±778 pg/ml). The difference between GHS children and children with idiopathic GHD was not significant. Klotho levels positively correlated with IGF-1- standard deviation scores (SDS) (R = 0.45, p<0.001), but were not associated with gender, pubertal status, age or anthropometric measurements.

Conclusions

We have shown, for the first time, an association between low serum klotho levels and organic GHD. If validated by additional studies, serum klotho may serve as novel biomarker of organic GHD.     

Fatherhood, pairbonding and testosterone in the Philippines

In species with a high level of paternal care, including humans, testosterone (T) is believed to help mediate the trade-off between parenting and mating effort. This hypothesis is supported by the observation of lower T in pairbonded men or fathers compared to single, non-fathers; however, prior work has highlighted population variation in the association between T and pairbonding or fatherhood status. Here we evaluate this hypothesis in a large (n = 890), representative birth cohort of young men (age range 20.5–22.5 years) living in Cebu City, the Philippines. Bioavailable T was measured in saliva collected prior to bed and immediately upon waking the following morning. Plasma T and luteinizing hormone (LH) were measured in morning plasma samples. In this sample, 20% of men were pairbonded, defined as living with a partner or married, 13% were fathers, and roughly half of fathers reported involvement in childcare. Pairbonded men had significantly lower T at both times of day. Unlike in other populations, this relationship was accounted for entirely by fatherhood status: among the large sub-sample of non-fathers, mean T was nearly identical among pairbonded and single men. There was a strong association between self-reported involvement in childcare and lower evening T, supporting the idea that the evening nadir in T is related to social interactions across the day. Similar relationships were found for total plasma T and LH, suggesting that these relationships are coordinated by centrally-mediated changes in LH secretion. The relatively modest T difference in relation to fatherhood at Cebu, in comparison to other studies, may reflect a lower level of paternal involvement in childcare activities in this population. Our findings using a large, well-characterized birth cohort support the hypothesized role of T as a mediator of mating and parenting effort in humans, while contributing evidence for cultural variation in the relative importance of pairbonding and fathering to these relationships.     

The Metabolic Syndrome and ECG Detected Left Ventricular Hypertrophy – Influences from IGF-1 and IGF-Binding Protein-1

Background and Aims

The metabolic syndrome (MetS) is associated with an increased risk for left ventricular hypertrophy (LVH) and cardiovascular mortality. The aim of this study was to investigate potential influences from insulin-like growth factor-1 (IGF-1) and IGF binding protein-1 (IGFBP-1) on the relationship between the MetS and LVH, also taking into account the role of physical activity (PA), use of oestrogen and gender.

Methods and Results

In a population-based cross-sectional study of 60-year-old men (n = 1822) and women (n = 2049) participants underwent physical examination and laboratory tests, including electrocardiography (ECG), and completed an extensive questionnaire. Women showed higher levels of IGFBP-1 than men (37.0 vs. 28.0 µg/l, p<0.001), and women with LVH had lower levels of IGFBP-1 than women without LVH (31.0 µg/l vs. 37.0 µg/l, p<0.001). Furthermore, women with low levels of IGFBP-1 had a significantly increased risk of having LVH (crude OR≈2.5). When stratifying for PA and oestrogen, respectively, a weaker association between IGFBP-1 and LVH was demonstrated in physically active men and women, compared to inactive individuals, as well as in women using oestrogen, compared to non-users.

Conclusion

In a representative sample of 60-year-old Swedish men and women, the main findings were higher levels of IGFBP-1 in women than in men; lower levels of IGFBP-1 in women with LVH, compared to women without LVH; and an increased risk of having LVH in women with low levels of IGFBP-1. The association between IGFBP-1 and LVH was diminished in physically active men and women, as well as in women using oestrogen.     

Soluble Endoglin,Transforming Growth Factor-Beta 1 and Soluble Tumor Necrosis Factor Alpha Receptors in Different Clinical Manifestations of Preeclampsia

Background

Despite intensive research, the etiopathogenesis of preeclampsia (PE) remains uncertain. Inflammatory and angiogenic factors are thought to play considerable roles in this disease. The objective of this study was to investigate the association between soluble endoglin (sEng), transforming growth factor beta-1 (TGF-β1) and tumor necrosis factor alpha soluble receptors (sTNF-Rs) and the clinical manifestations of PE.

Methods

Plasma levels of sEng, TGF-β1 and sTNF-Rs were determined by ELISA in 23 non-pregnant, 21 normotensive pregnant and 43 PE women. PE women were stratified into subgroups according to the severity [mild (n = 12) and severe (n = 31)] and onset-time of the disease [early (n = 19) and late (n = 24)].

Results

Pregnancy was associated with higher levels of sEng, sTNF-R1 and sTNF-R2 than the non-pregnant state. Moreover, PE women had higher levels of sEng and sTNF-R1 than normotensive pregnant women. No difference was found in TGF-β1 levels, comparing the three study groups. Late PE had higher levels of sTNF-R1 and sTNF-R2 than early PE. No significant differences were found in sEng and TGF-β1 comparing early and late PE. sEng levels were higher in severe PE than in mild PE and no difference was found for TGF-β1, sTNF-R1 and sTNF-R2 levels. There was a positive correlation among sEng, TNF-R1 and sTNF-2 levels. Logistic regression analysis revealed that primiparity and sEng levels are independently associated with the development of PE. Furthermore, sEng levels are independently associated with the disease severity.

Conclusions

These results suggest that pregnancy is a condition associated with higher levels of anti-angiogenic and pro-inflammatory factors than the non-pregnant state and that PE is associated with an imbalance of these factors in the maternal circulation.