Developmental plasticity of human reproductive development: Effects of early family environment in modern-day France
Introduction
Humans acquire physical, social and cognitive competencies during an extended juvenile period [1], [2], which is highly dependent on adult caregiving [3], [4]. When the caretaking environment is modified, e.g., when one parent leaves and a stepparent arrives, child development may be affected. Associations between family conflict or the absence of a father with reproductive traits in children have been widely documented. In Western industrial societies, the absence of a father has been considered a risk factor for earlier onset of puberty, sexual activity, teen pregnancy and unstable marriages [5], [6], [7], [57]. Additionally, parental conflict during childhood is associated with earlier onset of puberty, earlier age of heterosexual dating and higher number of sexual partners [6], [8], [9].
Marital conflicts appear to be a key indicator for reproductive traits in children, although both the absence of a parent and the presence of a stepparent may account for these observations. Often following parental division is the arrival of a stepparent. Remarriage occurs more often in pre-industrial societies than in industrial societies because of higher mortality risks [10], [11], but the frequency is currently increasing in industrial societies as well. Children raised in a stepfamily often receive less general investment [12], both educational and financial [13], [14], [15], [16], [17] than children raised by both of their biological parents. Stepchildren express more physiological [18] and psychosocial stress [19], and tragically, are at higher risks for infanticide [20], [21] and sexual abuse [22], [23], [24].
The presence of a stepfather may be associated with a reduced investment, and is therefore expected to increase costs associated with the absence of a father. A brief review of studies comparing these two effects is presented in Table 1. Studies testing the effects of the absence of a father vs. the presence of a stepfather has led to contradicting results concerning the age of puberty onset: three studies have claimed that the presence of a stepfather has an effect on the age of puberty onset [25], [26], [58], while another study shows no effect [27] (Table 1). Unexpected or unusual results require replication, such as the observation that the presence of a stepfather is associated with an earlier age of first sexual intercourse in women but not with a higher number of sexual partners compared to when a father is absent [26]. As most studies focus only on women, the effect of a stepfather on male reproductive development has not been extensively studied. Even if women are more sensitive to the trade-off between allocations of resources for physical growth vs. production of offspring [28], there may also be important family context effects on male reproductive developmental outcomes. Finally, the developmental outcomes of children from various parental environments have not been studied in a broad range of cultures, limiting the general applicability of the results (Table 1). Thus, we first aimed to clarify the specific effects of the absence of a father and the presence of a stepfather, investigating the details of timing sensitivity to these two factors.
Flinn and England have shown that the absence of a father, and to a further extent the presence of a stepfather, leads to a rise of cortisol levels in children [29]. Cortisol is a key hormone produced in response to physical and psychosocial stressors and modulates a wide range of somatic functions including energy release, immune activity, mental activity, growth, and reproductive function [30]. To our knowledge, the effects of the absence of a father and the presence of a stepfather on reproductive hormones have not been investigated. The levels of circulating testosterone in both men and women are associated with responses to competitive situations and social dominance, facilitating direct competitive behaviors such as aggression [31], [32], [33], [34]. Testosterone levels can be considered as a proxy for the capacity to compete for access to mates [32], [35].
However, sex differences are observed in endocrine patterns. Women produce one-fifth to one-seventh the levels of testosterone in men, and the link between competition and testosterone is contingent on the perception of losing or winning for men, but not for women [32]. Sex differences could be better understood in the context of life history strategies. For men, testosterone levels reflect the investment between parenting and mating, with higher testosterone levels associated with a higher investment in seeking copulations. The endocrine pattern in males is sensitive to social context: Marriage and fatherhood are associated with a decrease in testosterone levels in men [36], [37], [38]. According to Belsky's hypothesis, men who experience a rearing environment where the father is absent would shift to a mating strategy, leading to an increase in testosterone levels [39]. Additionally, in response to competition with other males, such as stepfathers, males are predicted to show an increase in testosterone levels. The second aim of this paper is to investigate whether parental separation is related to changes in testosterone levels of offspring.
Although previous studies have established a clear link between familial environment and traits potentially associated with reproductive success, none have actually measured fitness outcomes resulting from such family configurations. The challenge here is to understand the nature of these changes: are these changes plastic and adaptive responses to a change in the family environment or merely an expression of the costs of developmental perturbations?
Among current theories, some hypothesize that the observed changes are adaptive responses and consider them constrained and costly. Draper and Harpending posit that early experiences concerning fathering and marital relationships influence the reproductive strategy that individuals develop in adulthood [40]. As the expression of paternal investment is variable, it is in the child's interest to use environmental cues to assess the potential for paternal investment and adjust their future reproductive strategies accordingly. In particular, the absence of a father causes girls to advance sexual maturation and express higher sexual interests, which would be advantageous in an environment with low paternal investment. Belsky, Steinberg, and Draper state that children respond adaptively to many aspects of their rearing environments (e.g., poverty, the absence of a father, divorce) and are especially sensitive to events occurring during the first years of life [39]. They propose that early experience allows assessment of various environmental components (i.e., predictability and availability of resources, trustworthiness of others), which, in turn, affects reproductive strategy. From these foundations, Ellis focused on the influence of fathering and raised questions about the possible mechanisms by which fathers (either their physical presence or the quality of their investment) influence the onset of puberty in girls [5], [28]. Note that these theories rely on the assumption that variations in paternal investment are sufficiently low among fathers within a population and that the level of paternal investment is sufficiently stable, and therefore predictable, in a given population.
Parental separation could also result in a reduction of parental investment. This would lead to those individuals who suffered the costs of a reduced investment to start reproducing earlier, in order to lengthen their reproductive life and therefore increase their total number of offspring [41]. Indeed, several reproductive strategies in humans, as in other animals, are based on the allocation of resources between quantity and quality of one's offspring [59], [42]. The third aim of the present study is to clarify this situation and directly measure fitness outcomes using the best available estimators, number of children and grandchildren.
We first analyzed the effects of the absence of a father and the presence of a stepfather at various stages during childhood using a large panel of reproductive traits, including behavioral and physiological traits. We then tested whether family changes were associated with a decrease in fitness, and determined if the costs were compensated by plastic adaptive responses. We have thus investigated the influence of family changes on several reproductive traits and fitness measures using a retrospective study of childhood experiences.
In the first study (Study A), we surveyed a French student population comprised of young adults raised in three types of families: two biological parents, mother alone, or mother and stepfather. The age of menarche and age of first sexual intercourse (both related to length of reproductive period), as well as the number of sexual partners were reported. Additionally, the timing sensitivity to the absence of a father and the presence of a stepfather on the child's developmental traits was controlled. In a subsample of the same student population, we used saliva samples to assess physiological data on testosterone levels.
In the second study (Study B), the long-term effects of parental separation on the number of children and grandchildren were tested on a large sample of middle-aged adults participating in a longitudinal study on adult health.
Section snippets
Study A
In December 2004, anonymous questionnaires were completed by 1200 arts or sciences students from all academic levels at the University of Montpellier. Participation was voluntary, and all subjects were informed about the confidentiality and general aim of the study (effect of familial environment on various reproductive traits). Data on family characteristics and reproductive traits were recorded. Students were asked to detail their family compositions between 0 and 15 years of age, including
Results
Descriptive data and statistical models on the relationship between family composition and reproductive traits in children are shown in Table 2, Table 3, respectively.
What are the relative effects of the absence of a father and the presence of a stepfather at different stages during childhood on reproductive traits?
This study examined the link between modifications of family structure and parental separation. In particular, we investigated the role that the absence of a father and the presence of a stepfather played on reproductive development, behavior and physiological traits of the offspring.
Conclusion
Our results suggest that the relationship between changes in family composition and reproductive traits of children are likely to result from a combination of environmental and genetic factors. Reproductive outcomes of individuals partly or completely raised in the absence of a father may be only due to a genetic correlation between the father's behavior and the children's reproductive traits, possibly misunderstood if considered a priori as costs. However, some effects are surely due to a loss
Acknowledgments
We thank M. Flinn, B. Crouau-Roy, L. Chikhi and three anonymous reviewers for helpful comments on this manuscript. We are also grateful to the team RPP-C of Cetaf-Inserm U687, the students and teaching staff at the University of Montpellier and the GAZEL volunteers who participated in the study. IBL, Hamburg provided technical support; E. Kerinec, N. Guyot and V. Metz assisted with the survey, and V. Durand helped with the bibliography. Contribution 2008.082 of the Institut des Sciences de
Alexandra Alvergne is a Ph.D. student at the University of Montpellier II, France. In addition to the impact of family composition on child development, her research focuses on paternal investment and paternity uncertainty.
References (59)
Does father absence place daughters at special risk for early sexual activity and teenage pregnancy
Child Development
(2003)- et al.
Father absence, menarche and interest in infants among adolescent girls
Developmental science
(2004) Male care and mating effort among Hadza foragers
Behavioral Ecology and Sociobiology
(1999)- et al.
Paternal care by genetic fathers and stepfathers I: reports from Albuquerque men
Evolution and Human Behavior
(1999) Educational attainment of siblings in stepfamilies
Evolution and Human Behavior
(2001)- et al.
Parenting other men's children. Costs, benefits, and consequences
- et al.
Male–female differences in effects of parental absence on glucocorticoid stress response
Human Nature
(1996) Some differential attributes of lethal assaults on small children by stepfathers versus genetic fathers
Ethology and sociobiology
(1994)- et al.(1988)
The prevalence and seriousness of incestuous abuse: stepfathers vs. biological fathers
Child Abuse & Neglect
(1984)
Age at puberty and father absence in a national probability sample
Journal of adolescence
Father absence, parental care, and female reproductive development
Evolution and Human Behavior
Psychosocial antecedents of variation in girl's pubertal timing: maternal depression, stepfather presence, and marital and family stress
Child Development
Testosterone, cortisol, and women's competition
Evolution and Human Behavior
Dominance and testosterone in women
Biological Psychology
Human male pair bonding and testosterone
Human Nature
Marriage and fatherhood are associated with lower testosterone in males
Evolution and Human Behavior
Hormonal correlates of human paternal interactions: a hospital-based investigation in urban Jamaica
Hormones and Behavior
Father absence and reproductive strategy: an evolutionary perspective
Journal of Anthropological Research
Statistical computing: an introduction to data analysis using S-Plus
Why father absence might precipitate early menarche. The role of polygyny
Evolution and Human Behavior
Parent–daughter transmission of the androgen receptor gene as an explanation of the effect of father absence on age at menarche
Child Development
Behavior programs and evolutionary strategies
American Scientist
Evolutionary developmental psychology
Child Development
Evolutionary hypotheses for human childhood
Evolutionary Psychology, The new science of the mind. Boston
Behavioral ecological implications of early hominid body size
Journal of Human Evolution
Childhood stress, behavioural symptoms and mother–daughter pubertal development
Journal of Adolescence
Retrospective survey of parental marital relations and child reproductive development
International journal of behavioral development
Family relations in early childhood and reproductive development
Journal of reproductive and infant psychology
Cited by (47)
Childhood adversity and accelerated reproductive events: a systematic review and meta-analysis
2024, American Journal of Obstetrics and GynecologyFamily environmental antecedents of pubertal timing in girls and boys: A review and open questions
2022, Hormones and BehaviorCitation Excerpt :Father absence in particular was originally suggested to have its biggest impact on girls' pubertal timing when father absence occurs before age 5 (Ellis, 2004), but there was insufficient evidence to support or refute this. In some studies, pubertal timing was influenced by father absence only before age 5 (Culpin et al., 2014; Jones et al., 1972; Quinlan, 2003), but other studies reported effects of father absence effects at multiple developmental stages (Alvergne et al., 2008; DiLalla et al., 2021), including adolescence (Campbell and Udry, 1995). Other studies included a broad age range that prevented assessment of age effects.
Sexual initiation among Canadian youth: A model comparison approach of evolutionary hypotheses shows greatest support for extrinsic mortality cues, intergenerational conflict, and early life psychosocial stressors
2020, Evolution and Human BehaviorCitation Excerpt :There is debate as to whether father absence plays a unique role in reproductive scheduling (Ellis, 2004; Ellis, Bates, Dodge, et al., 2003) or if it simply indicative of psychosocial stress associated with divorce and growing up in a single-parent (or step-parent) household (Belsky et al., 1991). Evidence has shown that father absence in childhood is associated with earlier age at menarche for girls (Alvergne, Faurie, & Raymond, 2008; Bogaert, 2005; Moffitt et al., 1992; Quinlan, 2003; Webster, Graber, Gesselman, et al., 2014) and puberty for boys (Bogaert, 2005; Sheppard & Sear, 2012), as well as earlier age at first sex (Alvergne et al., 2008; Ellis et al., 2003; Newcomer & Udry, 1987; Quinlan, 2003) and earlier age at first birth (McLanahan & Bumpass, 1988; Nettle et al., 2010; Quinlan, 2003; Sheppard & Sear, 2012). Unfortunately, some of these results are not consistent.
Family dynamics and age-related patterns in marriage probability
2020, Evolution and Human BehaviorWhat the future held: Childhood psychosocial adversity is associated with health deterioration through adulthood in a cohort of British women
2014, Evolution and Human BehaviorCitation Excerpt :Tracy Chapman, Fast Car A large corpus of work has shown that women who experience childhood psychosocial adversity tend to go on to exhibit relatively early menarche, sexual debut, and first pregnancy (e.g. Alvergne, Faurie, & Raymond, 2008; Belsky, Steinberg, & Draper, 1991; Belsky et al., 2007; Chisholm, Quinlivan, Petersen, & Coall, 2005; Ellis et al., 2003; Nettle, Coall, & Dickins, 2011; Pesonen et al., 2008; Tither & Ellis, 2008). This acceleration of reproductive schedule in response to childhood psychosocial adversity has been viewed as an evolved adaptive response, rather than as a consequence of system dysregulation (Belsky et al., 1991; Chisholm, 1993; Ellis, Figueredo, & Schlomer, 2009).
Alexandra Alvergne is a Ph.D. student at the University of Montpellier II, France. In addition to the impact of family composition on child development, her research focuses on paternal investment and paternity uncertainty.
Charlotte Faurie is a research scientist of the CNRS of the University of Montpellier II, France. Her theoretical interests include the human family, focusing on the evolution of cooperation between siblings.
Michel Raymond is a research scientist of the CNRS of the University of Montpellier II, France. His research focuses on sexual preferences, parental investment and social cognition.