Family Environmental Antecedents of Pubertal Timing in Girls and Boys: A Review and Open Questions

Holly T Pham; Lisabeth F DiLalla; Robin P Corley; Lorah D Dorn; Sheri A Berenbaum

doi:10.1016/j.yhbeh.2021.105101

. Author manuscript; available in PMC: 2023 Feb 3.

Published in final edited form as: Horm Behav. 2022 Feb 3;138:105101. doi: 10.1016/j.yhbeh.2021.105101

Family Environmental Antecedents of Pubertal Timing in Girls and Boys: A Review and Open Questions

Holly T Pham ^a, Lisabeth F DiLalla ^b, Robin P Corley ^c, Lorah D Dorn ^d,^e, Sheri A Berenbaum ^a,^e

PMCID: PMC9261775 NIHMSID: NIHMS1767114 PMID: 35124424

Abstract

Across nonhuman species, pubertal timing is affected by the social environment, with consequences for reproductive success and behavior. In human beings, variations in pubertal timing have not been systematically examined in relation to social environmental antecedents, although their psychological consequences are well documented. This paper focuses on links in human beings between pubertal timing and the childhood social environment, with several sections: A review of studies relating pubertal timing to the family context, a key aspect of the social environment; challenges in studying the issue; and opportunities for future work that takes advantage of and creates links with evidence in other species. The review shows that pubertal timing in girls is accelerated by adversity in aspects of the early family social context, with effects small in size; data in boys are not sufficient to enable conclusions. Inferences from existing studies are limited by variations in conceptualizations and measurement of relevant aspects of puberty and of the family social environment, and by methodological issues (e.g., reliance on existing data, use of retrospective reports, nonrandom missing data). Open questions remain about the nature, mechanisms, and specificity of the links between early family social environment and pubertal timing (e.g., form of associations, consideration of absence of positive experiences, role of timing of exposure). Animal studies provide a useful guide for addressing these questions, by delineating potential hormonal mechanisms that underlie links among social context, pubertal timing, and behavior, and encouraging attention to aspects of the social environment outside the family, especially peers.

Keywords: pubertal timing, early family context, early adversity

The pubertal transition is increasingly recognized to be important for psychological development. In human beings, changes in physical development induce psychological changes (e.g., normative increases in risk-taking, and symptoms of psychopathology in vulnerable youth) through effects of gonadal hormones and social experiences acting on developing neural systems (e.g., Braams et al., 2015; Forbes et al., 2010; Goddings et al., 2019; Ladouceur et al., 2019; Steinberg, 2008). Variations in the timing of those physical changes are associated with psychological problems during adolescence, in some cases continuing into adulthood. In particular, early puberty in girls is associated with risk for depression, delinquency, substance use, and early sexual activity (see discussions in, e.g., Graber, 2013; Hamlat et al., 2019; Negriff & Susman, 2011; Ullsperger & Nikolas, 2017). Variations in pubertal timing are also associated with adult health and illness, including cancer and cardiovascular disease (Daniel & Balog, 2009; Karapanou & Papadimitriou, 2010). Additionally, links between pubertal timing and outcomes are seen in nonhuman species, and variation may have important consequences for later behaviors. For example, delayed puberty is associated with more submissive and less affiliative group behaviors in rhesus macaques (Pincus et al., 2021).

Puberty is largely under genetic control (Aylwin et al., 2019; Styne & Grumbach, 2016), but aspects of pubertal processes can be altered by extreme perturbations in the psychological and physical environment. For example, pubertal onset in girls is accelerated by severe physical or sexual abuse in childhood (Boynton-Jarrett et al., 2013; Colich et al., 2020; Noll et al., 2017), and delayed by high levels of exercise (Warren, 1980); there are no comparable studies in boys. The social environment also affects pubertal development in nonhuman species, although effects may vary across species, partly in relation to family structure. This work is reviewed elsewhere (e.g., Cameron, 2011; Ellis, 2004; Hughes, 1982; Stephens & Wallen, 2013; Vandenbergh, 1983) and discussed later in the paper in relation to studies in human beings.

How Do Typical Variations in the Early Family Context Affect Pubertal Development?

A key question concerns the extent to which typical variations in pubertal development have their origins in typical variations in human childhood experiences (e.g., Belsky et al., 1991; Ellis, 2004). Taking perspectives from sociobiology, behavioral ecology, and modern evolutionary theory, Belsky and colleagues (1991) theorized that early experiences influence reproductive strategy through effects on pubertal development. In essence, they hypothesized that environmental context, marked by early experiences, especially family structure and parenting, provides clues to individuals about the likelihood of their future reproductive success, which is reflected in their pubertal timing. The salient experiences are thought to occur during the first 5 to 7 years of life and operate by facilitating the development of schemas regarding resources and relationships. Early experiences in stressful family environments associated with insecure attachments to caregivers are hypothesized to accelerate puberty by signaling unpredictable resources and unstable relationships; reproductive success is maximized in this situation by early sexual maturity. Conversely, early experiences in non-stressful family environments with secure attachments to caregivers are hypothesized to indicate predictable resources and stable relationships, and thus no need to mature and reproduce early.

Ellis (2004) subsequently modified and elaborated the work of Belsky et al. (1991) by suggesting that the focus should be on pubertal development itself rather than reproductive strategy, given that the latter is more distal from early experiences than is the former. Ellis viewed variations in pubertal timing as reflecting variations in the length of childhood resulting from childhood experiences. Hypothesized mechanisms are evolutionary in nature (as for Belsky et al., 1991), with early childhood environments serving as signals about the nature of future environments. Although Belsky et al. did not address sex differences, Ellis suggested that early experiences affected reproduction of females more than of males given sex differences in the importance of resources for reproduction.

Considerable work has focused on the association between typical variations in early experiences and pubertal timing. Some evidence supports the hypothesis that unfavorable early experiences in the family are associated with earlier puberty within the normal range, but links are not consistently found, and the relevant family factors vary across studies (and sometimes within study). Previous reviews focused almost exclusively on girls, concluding that timing of puberty (generally measured by age at menarche) is accelerated by an adverse family environment, such as father absence or lack of involvement, whereas puberty is normative in the context of a positive family environment (Allison & Hyde, 2013; Belsky, 2010, 2012; Belsky & Shalev, 2016; Canelón & Boland, 2020; Daniel & Balog, 2009; Ellis, 2004; Karapanou & Papadimitriou, 2010; Mishra et al., 2009; Posner, 2006; Webster et al., 2014; Yermachenko & Dvornyk, 2014; Zhang et al., 2019).

Limitations in previous reviews led us to revisit this issue. In particular, additional attention is needed to describe the magnitude of effects and the extent to which the effects vary across aspects of the family environment (including characteristics of parents), the child’s age when the events occur, the child’s sex, and methodological aspects of the study, especially whether data were obtained prospectively versus retrospectively, and geographic location. These points are elaborated in the next section. Examination of both empirical studies and reviews made clear many of the ambiguities involved in work on the topic. Therefore, in order to advance research in this field, we used this review as an opportunity to identify challenges and raise questions about the nature and mechanisms of links between the early family environment and pubertal timing; this discussion follows the review.

Evaluating Early Family Context Effects on Pubertal Timing

Our goals were two-fold: to conduct a narrative review extending previous work in human beings and synthesizing findings on the nature of the relation between the early family social context and pubertal timing, and to identify gaps and opportunities for future research. Throughout, we focused on typical variations in the family environment that were central to the foundational work of Belsky, Ellis, and colleagues. Studies included are listed in Table 1 and separated into panels (A-D) by country and nature of data collection, as detailed below. Following our assessment of human studies on early family environment links to pubertal timing, we addressed open questions that researchers should consider and highlighted how future human research can build on evidence linking social context and pubertal development in nonhuman animals.

Table 1.

Studies Examining Family Context Effects on Pubertal Timing in Girls and/or Boys

A. Studies Conducted in North America Using Prospective Measures

Study	Family Context Measure	Earlier Age at Menarche	Earlier Pubertal Timing: Girls	Earlier Pubertal Timing: Boys


Campbell & Udry, 1995^a N = 518 girls	FA: (5 years)	+0.10



Ellis et al., 1999 ^c	FA: (4–5 years)		+0.35^*
N = 173 girls	FE: Parental dyad conflict (12 months–5 years)		−0.22
	Negative family relationships (4–5 years)		−0.19
	Parental dyad supportiveness (4–5 years)		+0.52^*
	Positive family relationships (4–5 years)		+0.83^*
	PCI: Discipline harshness (4–5 years)		+0.08
	Mother coercive control (4–5 years)		+0.47
	Father coercive control (4–5 years)		−0.45
	Mother affectionate-positivity (4–5 years)		+0.61^*
	Father affectionate-positivity (4–5 years)		+0.95^*



Maestripieri et al., 2004^a N = 83 girls	FA: (birth–current (11–14 years))	+0.65^*



Belsky, Steinberg, et al., 2007 N = 397 girls, 359 boys	FA: (0–54 months)	+0.24	−0.20	+0.18
	(1^st–3^rd grade)	+0.24	−0.10	−0.22
	PCI: Mother conflict (54 months)	−0.14	+0.16	−0.14
	Mother conflict (1^st–3^rd grade)	−0.10	−0.12	−0.12
	Father conflict (54 months)	−0.16	−0.20	+0.14
	Father conflict (1^st–3^rd grade)	−0.14	−0.12	+0.14
	Mother harsh control (54 months)	+0.32^*	−0.12	−0.12
	Mother harsh control (1^st–3^rd grade)	+0.41^*	+0.24	+0.12
	Father harsh control (54 months)	+0.24	−0.16	+0.16
	Father harsh control (1^st–3^rd grade)	+0.24^*	−0.24	+0.24
	Mother sensitivity (6–54 months)	+0.20	−0.24	+0.10
	Mother sensitivity (1^st–3^rd grade)	+0.14	−0.28	−0.22
	Father sensitivity (6–54 months)	−0.20	+0.32	+0.14
	Father sensitivity (1^st–3^rd grade)	−0.22	−0.20	−0.14
	Mother closeness (54 months)	−0.14	−0.18	−0.18
	Mother closeness (1^st–3^rd grade)	−0.26	−0.28	+0.12
	Father closeness (54 months)	+0.18	−0.18	+0.12
	Father closeness (1^st–3^rd grade)	−0.20	−0.30	+0.10

Belsky, Houts, et al., 2010^c N = 373 girls	PCI: Attachment security (15 months)	+0.25^*	+0.32^*

Belsky, Steinberg, et al., 2010 N = 526 girls	PCI: Mother harshness (4.5 years)	+0.47

Sung et al., 2016 N = 492 girls	PCI: Attachment security (15 months)	+0.28^*



Ellis & Essex, 2007 N = 180 girls	PCI: Mother supportiveness (3.5 & 4.5 years)		+0.61^*
	Father supportiveness (3.5 & 4.5 years)		+0.30

Rudolph & Troop-Gordon, 2010^a N = 86 girls, 81 boys	PC: Mother lifetime depression up to when child was 11 years		+0.12	−0.12



Arım et al., 2011 N = 4127 girls, 4313 boys	FA: Single-parent family (4–11 years)		−0.02	−0.02



Deardorff et al., 2011^c N = 444 girls	FA: (6–8 years)		+1.70^*^†



Jean et al., 2011^a N = 523 girls	FA: (childhood)	+0.49^*



DiLalla et al., 2021^c N = 328 girls, 405 boys	FA: (4–5 years)	+0.34^*	+0.19	−0.09
	(6–7 years)	+0.37^*	+0.18	±0.05
	FE: Family conflict (1–3 years)	+0.13	±0.05	−0.23
	Family conflict (5 years)	+0.50^*/⁰	+0.18	−0.10
	Family cohesion (1–3 years)	+0.14	±0.01	±0.24^*/°
	Family cohesion (5 years)	±0.14	−0.24	+0.19
	PCI: Harsh parenting/Low sensitivity (1–3 years)	+0.11	±0.12	+0.40^*/⁰
	Harsh parenting/Low sensitivity (4–5 years)	−0.12	−0.15	±0.05
	Harsh discipline (6–7 years)	−0.10	−0.13	±0.09
	Parent positive emotional tone (1–3 years)	−0.05	−0.14	−0.03
	Parent positive emotional tone (5 years)	+0.10	±0.10	+0.12
	Parent positive emotional tone (7 years)	+0.30^*/⁰	+0.22	±0.11
	PC: Mother neuroticism	+0.31^*/⁰	+0.37^*/⁰	−0.22
	Father neuroticism	+0.42^*/⁰	+0.31^*/⁰	±0.05
	Mother impulsivity	−0.14	+0.22	+0.49^*
	Father impulsivity	−0.10	+0.07	+0.16

B. Studies Conducted in North America Using Retrospective Measures

Study	Family Context Measure	Earlier Age at Menarche	Earlier Pubertal Timing: Girls	Earlier Pubertal Timing: Boys



Surbey, 1990 N = 1247 girls	FA: (prior to menarche)	+0.28**



Kim & Smith, 1998b N = 268 women, 89 men	FA: (prior to spermarche)			+0.06^*
	FE: Parental marital conflict (birth–7 years)	+0.35		+0.68^*
	Parental marital relations (birth–7 years)	+0.35^*		+0.54



Miller & Pasta, 2000 N = 178 women	FE: Family affection (childhood)	+0.52^*



Quinlan, 2003 N = 10,847 women	FA: Parents separated (birth–5 years)	+1.80^*^†
	Parents separated (6–11 years)	+1.49^†



Matchock & Susman, 2006 N = 1938 women	FA: (prior to menarche)	+0.29^*



Manuck et al., 2011 N = 455 women	FE: Family conflict (childhood)	+0.20^*
	Family cohesion (childhood)	+0.18



Bleil et al., 2013 N = 650 women	FE: Family conflict (childhood)	+0.22
	Family cohesion (childhood)	+0.27^*
	Family expressiveness (childhood)	+0.27^*



Gillette & Gudmunson, 2014 N = 532 girls	FA: (0–18 years)	+0.28^*

Amir et al., 2016 N = 3606 women	FA: Lived with father (early life)	+0.33

Mendle et al., 2016 N = 6273 girls	FA: (before birth)	+0.02	+0.01
	(0–5 years)	+0.03	+0.01
	(6–13 years)	+0.01	+0.03^*
	PCI: Parent emotional harshness (0–6 years)	+0.03^*	+0.01

Gaydosh et al., 2018^b N = 2681 women	FA: (birth–7 years)	+0.16^*

TenEyck et al., 2019 N = 3073 girls	FA: (lifetime)		−0.02



Henrichs et al., 2014 N = 3288 women	FA: (birth–16 years)	+0.04
	PC: Mental illness (childhood)	+0.17^*



La Guardia et al., 2014 N = 342 women	FA: (birth–menarche)	+0.23^*



Ryan, 2015 N = 1822 girls	FA: (before birth)	+0.33^*
	(birth–5 years)	+0.11
	(6–13 years)	+0.07



Sheppard et al., 2015 N = 5573 women, 6897 men	FA: Parents divorced (birth–7 years)		−0.02	−0.19^*



Azcorra et al., 2018 N = 246 women	FA: (birth–8 years)	+0.12



Richardson et al., 2018 N = 342 women	FA: Temporary father departure (before menarche)	+0.37^*

C. Studies Conducted Outside North America Using Prospective Measures

Study	Family Context Measure	Earlier Age at Menarche	Earlier Pubertal Timing: Girls	Earlier Pubertal Timing: Boys



Moffitt et al., 1992^a N = 416 girls	FA: (birth–11 years)	+0.22^*
	FE: Family conflict (7 years)	+0.26^*



Boynton-Jarrett & Harville, 2012^ac N = 4524 girls	FA: (birth, 7, or 11 years)	±0.09
	PCI: Lack of supportive caregiving (7 or 11 years)	−0.14

Sheppard & Sear, 2012 N = 9596 boys	FA: (birth–7 years)			−0.04
	(7–11 years)			−0.06



Culpin et al., 2014 N = 5295 girls	FA: (birth–5 years)	+0.08^*
	(5 years and up)	+0.03
	PC: Mother antenatal depression	+0.13^*

Culpin et al., 2015 N = 3785 girls	FA: (birth–5 years)	+0.24^*



Kelly et al., 2017 N = 5839 girls	FA: Lone parent family (7 years)	+0.05
	PC: Mother’s psychological distress (7 years)	0



Gettler et al., 2015 N = 754 boys	FA: (birth–11.5 years)			+0.02

Kyweluk et al., 2018 N = 807 girls	FA: (birth–11.5 years)	+0.08



Lenárt et al., 2019 N = 1151 girls	FA: (7 years)	+0.16

D. Studies Conducted Outside North America Using Retrospective Measures

Study	Family Context Measure	Earlier Age at Menarche	Earlier Pubertal Timing: Girls	Earlier Pubertal Timing: Boys



Jones et al., 1972 N = 400 women	FA: (birth–5 years)	+0.36^*
	(6 years–age at menarche (8–18 years))	+0.05



Kiernan & Hobcraft, 1997 N = 2347 women	FA: Family disruption (birth–16 years)	+0.18

Bogaert, 2008 N = 5013 women	FA: (birth–16 years)	+0.16^*



Kim et al., 1997 N = 197 women, 183 men	FE: Parental marital conflict (birth–7 years)			+0.41
	Parental marital relations (birth-11 years)	+0.39
	PCI: Mother conflict (birth–7 years)	+0.41^*
	Father care (birth–11 years)	+0.41^*
	Mother emotional distance (birth–11 years)	+0.41^*
	Father emotional distance (birth–7 years)			+0.41



Kim & Smith, 1998a N = 28 girls	PCI: Mother conflict (birth–6 years)	+0.93
	Mother rejection (birth–6 years)	+0.93
	Mother closeness (birth–6 years)	+1.01^*



Kim & Smith, 1999 N = 341 women, 168 men	FE: Parental marital conflict (birth–11 years)	+0.45^*
	PCI: Mother emotional closeness (birth–11 years)			+0.45^*



Jorm et al., 2004 ^c	FA (birth–16 years)	+0.06^*/⁰
N = 3702 women	FE: Home conflict (birth–16 years)	+0.12^*
	PCI: Father lack of affection (birth–16 years)	+0.04
	Strict authoritarian upbringing (birth–16 years)	+0.06
	PC: Mother emotional trouble (birth–16 years)	+0.06^*
	Father emotional trouble (birth–16 years)	+0.12^*



Alvergne et al., 2008 N = 708 women, 270 men	FA: (0–5 years)	+0.22^*
	(5–10 years)	+0.30^*



Sheppard et al., 2014 N = 567 women	FA: (birth–7 years)	+1.32



van Brummen-Girigori & Buunk, 2015 N = 189 girls	FA: (birth–5 years)	+0.10
	(6–13 years)	+0.28



Smith, 2017^b N = 2297 girls	FA: (birth–6 years)	+0.20^*

Magnus et al., 2018 N = 8984 women	PCI: Mother lack of care (childhood)	−0.16
	Mother overprotection (childhood)	+0.10
	PC: Mental illness (childhood)	+0.16



Demakakos et al., 2019 N = 2383 women	PCI: Mother overprotection (birth–15 years)	−1.11^*^†
	Father overprotection (birth–15 years)	−1.10^*^†
	Mother care (birth–15 years)	+1.04
	Father care (birth–15 years)	+1.09

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Note. Adversity measures are categorized by the following constructs: Father Absence (FA), Family Environment (FE), Parent-Child Interactions (PCI), and Parent Characteristics (PC). Most effect sizes were converted to Cohen’s d. Hazard and risk ratios could not be converted to Cohen’s d and instead were kept as hazard and risk ratios and represented as (†). Effects in the expected direction (i.e., a negative environment is associated with earlier pubertal timing) are represented by (+). Effects in the unexpected direction (i.e., a negative environment is associated with later pubertal timing) are represented by (-). Null effects are represented by (0). Average effect size was calculated and included in the table when multiple effect sizes were reported for the same family context measure. Multiple effects for the same family context measure that had different directions (i.e., expected and unexpected) are represented by (±). Multiple effects for the same family context measure that had different significances are represented by (*/⁰).

Represents studies that included at least one measure of family context or pubertal timing that was retrospective.

Represents studies that included at least one measure of family context or pubertal timing that was prospective.

Represents studies that reported multiple effects for the same family context measure.

p < .05.

Focus of the Review

We focused on describing the size of effects and factors that might influence findings and that could be evaluated. Effect sizes (and directions) allowed us to assess consistency in the nature and direction of the factors contributing to early puberty, especially in studies with relatively small samples (moving beyond statistical significance of findings).

Several factors likely to affect the nature and size of the association were considered, summarized in Figure 1. First, we characterized the nature and measures of environmental experiences, focusing on normative early experiences rather than extreme events (e.g., abuse, neglect, trauma) because we were primarily interested in effects on puberty that occur within the confines of typical development. Although extreme events affect pubertal timing (Boynton-Jarrett et al., 2013; Colich et al., 2020; Noll et al., 2017), they also affect other aspects of development (e.g., nutrition) that could independently affect pubertal timing, and they may have highly diverse effects on pubertal timing by either delaying or accelerating it. Extreme events might also obscure small effects seen in typical environments.

Constructs Excluded and Included in Review

*Note*. Constructs shown are thought to influence pubertal timing. White boxes are constructs that were included in the review. Black boxes are constructs that were excluded from the review.

We focused on measures of key constructs characterizing aspects of the early childhood environment hypothesized to contribute to pubertal timing according to Belsky et al. (1991).¹ (Although there is no clear definition of “normative” experiences (Humphreys & Zeanah, 2015), we focused on events that are typically encountered by children, in line with Belsky et al.’s (1991) theory.) In previous reviews, the environment was often described broadly and included aspects that were not part of the original hypotheses. In some cases, family environmental effects were examined in the context of general risk factors for earlier pubertal timing; these included genetic and environmental factors such as prenatal growth (Fisher & Eugster, 2014), health and nutrition (Daniel & Balog, 2009), environmental contaminants (Daniel & Balog, 2009), illness (Karapanou & Papadimitriou, 2010), exposure to war (Karapanou & Papadimitriou, 2010), race (Posner, 2006), and climate change (Canelón & Boland, 2020). In other cases, psychosocial environmental influences were described in general terms (e.g., environmental stress, psychosocial factors, contextual adversity, family environment), or a broad category of environmental adversity was used that combined typical variations in the environment, such as parenting and quality of family relationships, with extreme events, such as physical or sexual abuse, and war conditions (Belsky & Shalev, 2016; Fisher & Eugster, 2014; Joos et al., 2018; Karapanou & Papadimitriou, 2010; Mishra et al., 2009; Posner, 2006; Yermachenko & Dvornyk, 2014; Zhang et al., 2019).

Therefore, returning to the foundational work (Belsky et al., 1991; Ellis, 2004), we focused on father absence or presence (presumed biological father), parent behaviors specific to the child (e.g., parental control, harsh discipline, maternal warmth to child), and general family function (e.g., conflict). We planned to examine separate aspects of parenting (e.g., warmth versus discipline) but were unable to do so because they were defined in different, and sometimes contradictory, ways across studies.

We also evaluated the role of parents’ characteristics. The childhood family environment depends in large part on parents who provide both environment and genes to their children. The key hypothesized influences on pubertal timing – father absence, parent-child interactions, and family function – are both a function of parents’ characteristics and an environmental context for children. Previous reviews have given little consideration to the possibility that the family environment is a reflection of parents’ characteristics. Therefore, we sought to determine whether pubertal timing was related to parents’ psychological health or personality.

We did not include socioeconomic status (SES) because it is a proxy for specific aspects of the environment that may have opposing effects on puberty; for example, food insecurity may delay puberty through malnutrition or accelerate puberty through obesity from a high fat diet, and parental stress from low SES may be linked in different ways to offspring’s pubertal timing through different mechanisms. As expected, previous reviews reported inconsistent links between SES and pubertal timing, reflecting the heterogeneity of SES and its range within a given sample (Ellis, 2004; Karapanou & Papadimitriou, 2010; Mishra et al., 2009; Xu et al., 2018; Yermachenko & Dvornyk, 2014).

Second, we considered the child’s developmental status when the event was experienced. The sensitive period may differ based on hypothesized mechanisms linking environment to puberty, e.g., infancy and toddler years based on attachment theory (Belsky, Houts, et al., 2010), infancy and preschool years based on the development of cognitive abilities necessary to understand and internalize events and on the demonstrated benefits of high-quality child care at these ages (Li et al., 2013), ages 5–7 years based on hypotheses about environmental events specifically related to reproductive outcomes (Belsky et al., 1991; Ellis, 2004). Furthermore, we restricted our review to studies clearly focusing on events occurring before puberty. We chose age 7 as our ceiling, given the typical range of pubertal onset and the need for events to have time to influence it. There has been little consideration in previous reviews of the ways that environmental effects on pubertal timing depend on the child’s age when the events were experienced (with the exception of Ellis, 2004; Xu et al., 2018); in some cases, environmental events were not even restricted to the prepubertal years (Allison & Hyde, 2013; Posner, 2006; Sear et al., 2019; Webster et al., 2014; Xu et al., 2018).

Third, we examined effects separately for boys and girls. Early environments are suggested to affect reproduction more in females than in males, but most work has been restricted to girls, preventing an assessment of the sex-specificity of effects, and thus the underlying mechanisms. Reviews that did consider boys were inconsistent or inconclusive, likely because of little empirical evidence in boys (Fisher & Eugster, 2014; Hummel et al., 2013; Joos et al., 2018; Sear et al., 2019; Xu et al., 2018). In one review, it was concluded that negative parenting was associated with earlier pubertal timing in girls but not boys, whereas increased parental support was associated with later pubertal timing in both girls and boys (Hummel et al., 2013); but this was based on limited evidence. Other reviews noted the paucity of studies examining effects in boys, which led to mixed findings (Joos et al., 2018; Sear et al., 2019).

Fourth, we considered the country in which the study was conducted. This is a rough proxy for cultural variations that might contribute to associations between family environment and pubertal timing. Ideally, the question of cultural variations would be examined within a single country (e.g., by race and ethnicity within the United States), but there was insufficient evidence to examine this, so we compared effects in studies conducted in North America versus other regions (United Kingdom, continental Europe, Southeast Asia, Oceania). Only one previous review (Sear et al., 2019) went beyond White and educated samples: early pubertal timing was inconsistently related to father absence. This might reflect the review’s inclusion of father absence due to migrant work (Chang & Lu, 2018), which is beyond the traditional conceptualization of father absence as family disruption.

Finally, we considered whether results varied by the prospective versus retrospective nature of data used to assess family environment, given the methodological limitations of retrospective reports (e.g., Loftus, 1975); for example, reports of childhood parenting obtained during adolescence and adulthood were shown to be modestly correlated (Bell & Bell, 2018). In the table, we note two caveats: In some studies, with prospective reports of the family context, some measures (such as menarcheal age) may have been obtained retrospectively; in some studies with retrospective reports of family context, puberty was assessed contemporaneously.

Studies in Table 1 are organized based on the latter two factors, that is, geographic region in which the study was conducted, and timing of data collection. Panels A and B list studies conducted in North American countries (e.g., United States, Canada, Mexico), using prospective and retrospective methods, respectively. Panels C and D list studies conducted outside North America (e.g., United Kingdom, Australia, Malaysia), again separated by prospective and retrospective methods.

Criteria for Inclusion

Studies were included in the review – and listed in Table 1 – if there was information on effect sizes for associations between early childhood family context and pubertal timing, either provided directly in the manuscript or able to be calculated from information provided (using online resources: Becker, 2000; Lenhard & Lenhard, 2016; Wilson, 2001). Effects were reported in the table without consideration of other variables examined. For example, a zero-order correlation between pubertal timing and father absence was listed even if the correlation was reduced when factors such as family constellation or parents’ personality were included; this facilitated comparisons across studies because other factors were not systematically examined across studies. It is important to note that several papers reported on similar or overlapping samples (with participant selection based on investigators’ interests or participants’ meeting specific criteria, e.g., race), so results of studies were not necessarily independent. Papers reporting on data from the same or overlapping samples were grouped together in the table, with double lines between studies from independent samples.

We included studies that provided sufficient information to test at least our main question about links between early family social context and pubertal timing; not all retained studies addressed all foci. Studies were excluded for one or more of the following reasons: (a) girls and boys were combined in analyses or sex/gender was controlled (no separate analyses by sex); (b) samples included participants in atypical circumstances (e.g., foster care, war, father absence due to migrant work) or had extreme adversity (e.g., maltreatment, sexual abuse); (c) experiences could not be easily categorized because they were not specific to the early family context as specified by Belsky et al. (1991) (e.g., emotional autonomy, behavioral independence, father absence included nonbiological fathers), were vague (e.g., household moves), were not analyzed separately but instead combined into a single composite measure (e.g., “stress”), or were assessed in a small number of studies (e.g., mother absence, stepfather exposure); (d) pubertal status only was reported (not timing), timing was atypical (e.g., precocious), or only adrenarche was assessed; (e) analyses combined samples across geographic region or split them in ways that made evaluation difficult (e.g., by race or ethnicity; by birth order); (f) were unpublished theses.

A difficult decision about inclusion of studies concerned timing of exposure to family adversity. Events that contribute to puberty must obviously occur before puberty, but a surprising number of studies failed to restrict environmental assessments to the prepubertal period. We tried to exclude results that were not limited to childhood (up to and including age 7), and were able to do that when reported events occurred in adolescence and beyond, but we retained studies that included measures of environmental adversity across ages from birth into adolescence, because they were common and included the hypothesized risk period.

Some studies included data that met the inclusion criteria as well as data that did not. Therefore, we included in the review all elements of studies with measures and age ranges relevant to the hypotheses being tested, and excluded elements that did not meet the inclusion criteria listed.

Interpreting Results

Published results were reported in different statistics [correlations (r or R²), group differences (d or f), odds ratios (OR), hazard or risk ratios (HR/RR)], which we used to determine effect size. We used online calculators (Becker, 2000; Lenhard & Lenhard, 2016; Wilson, 2001) to convert statistics to Cohen’s d for ease of interpretation in Table 1. Hazard and relative risk ratios could not be converted to Cohen’s d and thus were kept as hazard and relative risk ratios. When multiple effect sizes were reported for the same family context measure (e.g., twin replicate data, multiple pubertal timing measures), average effect size was reported. We used Cohen’s (1988) criteria for d and Olivier et al. (2017)’s criteria for hazard and relative risk ratios to interpret effect sizes, although criteria for interpreting effect sizes may vary (Sawilowsky, 2009). We interpreted effect sizes as follows: no effect (d = .00, HR/RR = 0.00), minimal effect (.00 < d < .20, 0.00 < HR/RR < 1.22), small effect (.20 < d <.499, 1.22 < HR/RR < 1.859), medium effect (.50 < d < .799, 1.86 < HR/RR < 2.99), and large effect (d ≥ .80, HR/RR ≥ 3.00).

Table 1 also shows direction of effects in relation to hypotheses. A plus sign (+) indicates support for hypotheses, showing a negative environment was associated with earlier puberty. A minus sign (−) indicates findings opposite to hypotheses, showing a negative environment was associated with later puberty. A plus-minus sign (±) was used when multiple effects were in different directions. An asterisk/zero (*/⁰) was used when one effect was significant whereas the other was not.

Evidence for Early Family Context Effects on Pubertal Development

Results of the review are summarized in Table 1, Panels A-D. Several conclusions can be drawn from those studies. In sum, effects were stronger and more consistent for girls than for boys (with more data for the former than the latter), with effects generally small in size; the most consistent predictor of pubertal timing in girls was father absence; there was also some evidence that pubertal timing in girls was influenced both by parents’ behaviors directed to the child and general family function. Effects were similar in studies using prospective and retrospective reports, and in studies conducted in North America and other countries, although all studies outside North America measured timing of puberty in girls only by age at menarche.

The bulk of the evidence indicates that the more stressful and unsupportive the family environment, the earlier girls mature. There were also some significant effects in the direction opposite to expectation, and there were a considerable number of nonsignificant effects. From the perspective of evaluating replication of findings, it is important to keep in mind that separate reports sometimes include the same or overlapping samples.

Effect Size

Studies varied considerably in sample size and thus statistical power to detect effects of family context on pubertal timing. Not surprisingly then, given bias to publish papers reporting significant effects, and reduced power with small samples, it is generally the case that larger effects were seen in studies with small samples than in those with large samples. Small effects in small studies were often not significantly different from zero, whereas significant effects in some large studies were very small. Overall, the evidence suggests that population effects are in the small range.

Type of Early Family Context

The most consistent evidence concerned father absence, which was associated with early puberty in girls. This finding accords with conclusions from a meta-analysis of pubertal effects of father absence (Webster et al., 2014), and extends it in several ways: considering pubertal timing in addition to age at menarche, restricting environmental influences to the prepuberty period, and examining effects of experiences at different developmental stages, as detailed below. A key question concerns the processes represented by father absence, e.g., family stress, reduced economic resources, parents’ personality; we return to this issue below.

Other specific aspects of the environment found to predict pubertal timing in girls and boys varied across studies and sometimes within study using the same sample. This is not surprising given the variations in family context hypothesized to be important and in the measurement of apparently similar constructs of the family, largely due to the reliance on data already collected. Furthermore, measures used were not independent, although correlations among them were reported infrequently (for exceptions, see DiLalla et al., 2021; Ellis et al., 1999; Ellis & Essex, 2007). Thus, the apparent primacy of one over another aspect of the environment in a particular study may simply reflect measurement reliability or sampling error.

Therefore, it was not possible to identify specific features of the environment that are most important. There was evidence for inverse associations between pubertal timing in girls and a variety of adverse family circumstances, both child-directed parent behaviors (e.g., harsh parenting and low warmth, especially from mothers), and general family function (e.g., family conflict, parents’ dyadic relationship). These features of the family context effectively capture the aspects of early childhood experiences that were hypothesized by Belsky et al. (1991) to provide signals of reproductive success, reflecting relationship qualities and resource availability in normative environments.

Parents’ Characteristics

Although effects of parents’ psychological health on offspring pubertal timing have also been called out for consideration by others (Allison & Hyde, 2013; Ellis, 2004; Karapanou & Papadimitriou, 2010; Mishra et al., 2009; Posner, 2006), the topic remains understudied. There was some evidence that girls’ pubertal timing was inversely related to parents’ psychological problems (Culpin et al., 2014; Henrichs et al., 2014; Jorm et al., 2004), and personality (DiLalla et al., 2021), although significant effects were not always found (Kelly et al., 2017; Magnus et al., 2018; Rudolph & Troop-Gordon, 2010); boys’ pubertal timing was seen to be inversely associated with parents’ difficult personality (impulsivity) in one study (DiLalla et al., 2021), but not with depression in another (Rudolph & Troop-Gordon, 2010).

Developmental Effects

There was insufficient information to enable identification of sensitive periods for effects of family context on pubertal timing in either girls or boys. The majority of effects described in the table involved measures of events not confined to specific ages, e.g., occurring any time between birth and 11 years of age. It is unlikely that early puberty would be elicited by events proximate in time (and not possible to be influenced by events occurring after), so effects likely reflect the stability of environmental measures with later events a proxy for early ones.

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 & Udry, 1995). Other studies included a broad age range that prevented assessment of age effects. Father absence does not seem to influence boys’ pubertal timing (Belsky, Steinberg, et al., 2007; DiLalla et al., 2021; Sheppard & Sear, 2012), but was not hypothesized to do so.

Other aspects of the family context were rarely studied in relation to the child’s age at exposure. Two exceptions produced inconsistent results: In one study, pubertal timing in girls was seen to be influenced in similar ways by harsh control occurring during the first four years of life and during grades 1 through 3 (Belsky, Steinberg, et al., 2007); in another study, pubertal timing in girls was linked to parent positive emotional tone at 7 years and family conflict at age 5 but not earlier or later (DiLalla et al., 2021).

Sex Differences

In girls, early adversity was consistently linked to earlier pubertal timing. Effects of early family context on pubertal timing were studied more often and were clearer in girls than in boys, likely as a result of the emphases of the early work in human beings (Belsky et al., 1991; Ellis, 2004) and relative ease of measuring puberty in girls versus boys. The few studies that examined the question in boys did not provide a clear picture: both significant and nonsignificant effects were not consistently in the expected direction (negative experiences linked to earlier puberty). As we consider below, several factors might contribute to null or contradictory findings in boys, as also noted by others (Fisher & Eugster, 2014; Hummel et al., 2013; Joos et al., 2018; Sear et al., 2019; Xu et al., 2018).

Conceptual and Methodological Issues in Evaluating Studies

A number of issues need to be considered in interpreting the findings summarized above. Many issues reflect the fact that no study was explicitly designed to test hypotheses about effects of early experiences on pubertal timing. This is expected given the time lag to puberty from the antecedent events. But, it means that study designs – from the choice of environmental events to examine, through the measurement of those events and the ages at which they occurred, to the nature and timing of puberty assessments – were not constructed to test the hypotheses. A likely consequence is the underestimation of effects. Some of these issues have been noted by others (e.g., Ellis, 2004; Sear et al., 2019; Webster et al., 2014), but generally not incorporated into empirical work.

Assessment of Puberty

Although all studies purported to measure pubertal timing, they varied in how it was conceptualized and assessed. Most studies had significant limitations in their measures, but unsystematic variation made it difficult to assess effects of measurement. First, there was little consideration of the meaning of pubertal timing, that is, whether it referred to onset of puberty or midpuberty: age at menarche reflects reproductive maturity, but broad measures of pubertal timing (e.g., summary score of different indicators) were generally not discussed in terms of the aspect of puberty considered to be important, with a few exceptions (Belsky, Steinberg, et al., 2007; Deardorff et al., 2011; DiLalla et al., 2021). Furthermore, most studies provided a single sample of a developmental process that has multiple components and includes tempo (the speed with which someone progresses from pubertal onset to complete maturity) as well as timing.

Second, pubertal timing and pubertal status were often confounded: puberty was generally assessed only once in a sample of participants varying in age across adolescence. For example, a 12-year-old girl who has not yet reached menarche could ultimately be on-time or a late maturer. The issue is not serious if the main concern is to identify early maturers and if participants are well beyond the age that is considered early; this is true for girls in most studies, but may not apply to boys in the few studies that included them. But, even where early maturers can be identified, analyses often fail to acknowledge the limited nature of the measure of pubertal timing, that is, that investigators are not evaluating the full range of pubertal timing and are using a measure that is not ratio or even interval.

Third, some studies involved retrospective reports of pubertal timing from adult participants, with unknown validity of those reports (see discussion in Dorn et al., 2013). Further complications were introduced in studies mixing such retrospective reports of timing from those who had completed puberty with concurrent reports from those in the middle of puberty (also confounding pubertal timing and status).

Fourth, pubertal development was most often assessed by self-reports (sometimes replaced or supplemented by parent-report); although such reports are widely used, their validity has been questioned, particularly if precise staging is the focus. They are most valuable when data are provided on multiple occasions (Beltz et al., 2014), but longitudinal data beyond menarcheal age were rarely available (except for Belsky, Houts, et al., 2010; Belsky, Steinberg, et al., 2007, 2010), and there was generally not systematic use of multiple reports of menarche. The gold standard – physical exams performed by trained health professionals – was used rarely (Belsky, Steinberg, et al., 2007). Others have discussed the strengths and limitations of different methods of assessment (e.g., Berenbaum et al., 2015; Dorn et al., 2006; Dorn & Biro, 2011; Mendle et al., 2019; Shirtcliff et al., 2009).

Assessment of Features of Family Context

Hypotheses and early work about family influences on pubertal timing allow for considerable variation in the conceptualization and measurement of the specific salient influences, and this was reflected in variation across studies in the operationalization of family context (also noted by Sear et al., 2019; Webster et al., 2014). First, experiences related to family context were defined in different ways, including the presence of negative experiences such as parental harshness and adverse events, the absence of positive experiences such as fathers in the home, and the presence of positive experiences such as family cohesion and parental warmth. Many studies involved both the presence of negative and positive experiences and the absence of positive experiences as different indicators of family context, although the experiences were defined and operationalized in different ways. The coding of the valence of an event varied across studies; e.g., a negative event, such as parental harshness, might have been reversed in scoring and considered a positive event. The responses obtained might not have included the whole range. In general, scaling issues were also often problematic, e.g., use of dichotomous versus continuous scales, lack of anchor points. These issues prevented the examination of differential prediction of puberty from different aspects of the environment.

Second, even with a clear specification of family context, data captured varied across studies. It was common to use parent-report of family context, but there was also child-report of family adversity and parenting experiences, with most of the latter involving retrospective self-report. Findings appear to be similar across these types of reporting. Direct behavioral observation of families was rare, and was usually combined with parent-report. In cases with multiple timepoints, measurement of family context varied across assessment point, e.g., ratings of interviews with mothers used at one timepoint, home observation at another timepoint, and parent questionnaires at still another timepoint.

Third, studies were limited in their ability to identify sensitive periods for experiential effects on pubertal timing. Most studies were either limited to a narrow developmental period and not compared to another period, or included assessments of the family context during a wide age period, potentially obscuring identification of sensitive periods. We excluded studies with assessments exclusive to the preteen or teenage years, when participants were likely already in puberty or close to it. Further complicating efforts to identify developmental effects, environmental measures in most studies could have reflected cumulative or continuing experiences.

Open Questions and Opportunities for Research

Despite conceptual and methodological limitations to research in this area, the weight of the evidence indicates that pubertal timing in girls is affected by early experiences in the family to a small degree; there is insufficient evidence in boys. Establishing this finding, however, is the first step in understanding this important developmental process. In the following sections, we discuss questions about the effects that provide opportunities to contribute to that understanding. We start with the practical challenges inherent in this research, and then continue to questions about the nature, mechanisms, and significance of the effects. We discuss how these questions could be answered by leveraging knowledge regarding social context influences on hormones, behavior, and reproductive functioning in nonhuman species.

Practical Challenges and Solutions

Availability of Prospective Data

Strong tests about pubertal effects of the early environment would be facilitated by studies specifically designed to test the hypotheses. This is a difficult task given the time interval between the relevant events and puberty, and the need to treat and measure puberty as a complex developmental process. An alternative is use of existing longitudinal data with registration of the variables to be used (Munafò et al., 2017). This could attenuate two concerns: Examination of a large number of variables that are intercorrelated but have different psychometric properties likely leading to selective reporting of results for variables that showed significant links to pubertal timing; and unclear conceptualization and measurement of the pubertal processes mostly likely to be affected by the family environment.

Sample Recruitment and Retention

Missing data can be problematic by reducing rigor and confidence in inferences regarding links between pubertal timing and family context, so it is important to describe missing data and approaches to adjusting for them. In the studies we reviewed, it was common for data to be missing, but it was not common to see descriptions of their nature and consequences. In fact, lost data often had to be inferred from comparisons of participant descriptions and results (e.g., initial sample sizes compared to tabled numbers or degrees of freedom in results). In a few studies, comparisons were made between participants with missing versus complete data. Although the differences were not always significant (likely owing to limited statistical power), a consistent pattern emerged: those who were missing data were more likely than those with data to have more environmental risk. Demographically, they were more likely to have younger mothers (Belsky, Steinberg, et al., 2007), come from families with lower SES (Arım et al., 2011; Belsky, Steinberg, et al., 2007, 2010; Culpin et al., 2015; DiLalla et al., 2021; Mendle et al., 2016; Sung et al., 2016), or be a member of a racial or ethnic minority group (Belsky, Steinberg, et al., 2010; Mendle et al., 2016; TenEyck et al., 2019). In terms of family characteristics, they were more likely to have parents scoring higher on problematic personality traits (DiLalla et al., 2021), to have absent fathers (Belsky et al., 2007; Belsky, Steinberg, et al., 2010; Culpin et al., 2015; Moffitt et al., 1992; but compare to TenEyck et al., 2019), to experience more paternal transitions (DiLalla et al., 2021; Sung et al., 2016), or to be in families with more conflict and less cohesion (DiLalla et al., 2021). In terms of child characteristics, they were likely to be less securely attached as infants (Sung et al., 2016), to have more problem behaviors (Arım et al., 2011; Rudolph & Troop-Gordon, 2010), or to have earlier puberty (Culpin et al., 2015).

Thus, data are not missing at random for the key variables of interest, with information most likely to be missing from families with the lowest quality family circumstances, because research participation is most challenging for those with limited psychological and economic resources. Their loss affects more than generalizability – it essentially eliminates the families most likely to reflect the risk hypothesized to be associated with early puberty (or at least reduces their number), and substantially limits the ability to see effects. This suggests that associations between typical variations in the family environment and pubertal timing in girls are larger than have been reported.

Inclusion of Boys

Fewer than 20% of studies reviewed included boys (an issue also discussed by Deardorff et al., 2019; Joos et al., 2018; Mendle et al., 2019). Their exclusion likely reflects two issues: the emphasis of evolutionary perspectives on girls, and the relative difficulty of assessing puberty in boys compared to girls. Their inclusion in future studies could help to determine the specificity of environmental influences, and delineate mechanisms, as discussed below.

Determining the Nature of the Effects

Initial hypotheses and subsequent work focused on the consequences for pubertal timing of both ends of a continuum of childhood experiences. On one end, stressful family environments with insecure attachments to caregivers have been hypothesized to signal unpredictable resources and unstable relationships, leading to accelerated puberty. On the other end, non-stressful family environments with secure attachments have been hypothesized to indicate predictable resources and stable relationships, with minimal effect on expected pubertal timing. But studies have generally failed to consider both ends equally, and leave open many questions about the nature of the association.

The Meaning of Father Absence

Father absence is the most consistent predictor of pubertal timing in girls, but its meaning requires further study. For example, it could be a cause or consequence of psychological dysfunction in the family, perhaps related to interparental conflict, parents’ personality, a reflection of reduced economic resources available to the child, or the presence of unrelated males. Data on the presence of stepfathers could help distinguish alternatives, but these data are currently insufficient to determine specific father influences on pubertal timing (Clutterbuck et al., 2015; Steppan et al., 2019). Other productive approaches might include examination of effects of stepbrothers, especially postpubertal ones (testing effects of unrelated males in the home), and father absence due to death (e.g., military samples) versus divorce (reducing effects of parents’ problematic personality). It would also be valuable to understand the extent to which earlier puberty in adopted girls (Brooker et al., 2012; Mason & Narad, 2005; Teilmann et al., 2006; Virdis et al., 1998) is due to living with an unrelated male, e.g., by examining age at adoption, presence of other unrelated males.

The Form of the Association

Most studies involve continuous measures of environmental risk and puberty, with tests of their association based on linear models. It is possible – perhaps likely – that the effects are nonlinear, however. For example, there may be a threshold above which variations in environment do not affect puberty, with a certain level of environmental support being “good enough” (Scarr, 1992).

Positive vs. Negative Experiences

In many cases, the continuous environmental measures are also bipolar (with the ends anchored by negative and positive experiences), making it unclear if risk for early puberty arises from the presence of negative experiences or the absence of positive ones, or whether an adverse environment represents risk for early puberty or a supportive environment represents protection from it or even late puberty. It seems more likely that environmental adversity confers risk (for early puberty) than that a fully supportive environment is beneficial (for typical pubertal timing), but this has not been documented.

The little evidence comparing pubertal effects of positive versus negative experiences is inconclusive. In one study, pubertal timing in girls was seen to be significantly associated with positive but not most negative family relationships (Ellis et al., 1999). In another study, the results varied within and across measures of parenting and puberty (Belsky, Steinberg, et al., 2007). Links between pubertal timing and positive versus negative experiences were not statistically compared in either study. It is unclear if mixed findings reflect measurement issues (e.g., differential reliability) or even whether predictors were significantly different.

In the broader literature, positive and negative parenting behaviors are often considered on a continuum but measured as separate constructs, with a review showing that both the presence of harsh parenting and the absence of parental warmth and support increased risk for behavior problems in children (Hoskins, 2014). The two “ends” of parenting – parental harshness versus warmth and sensitivity – are correlated to a small to moderate degree (e.g., −.14 to −.27; Bradley & Corwyn, 2007; Waller et al., 2015), arguing for the value of future work testing the relative effects on puberty of positive versus negative experiences (and statistical comparisons of the associations). In doing so, it is again important to consider whether parenting effects on behavior problems are linear or not.

Accumulation of Adverse Experiences

Most studies have focused on individual environmental events in effects on pubertal timing, but it is likely that effects are cumulative and synergistic. In the one study that examined additive effects (Moffitt et al., 1992), age at menarche was not significantly better predicted from the combination of family conflict, behavior problems, and father absence than from the latter alone; this may reflect correlations among the predictors and differential measurement reliability. Examination of interactions with early experiences has been limited to demographics or temperament, with no consideration of interactions among the experiences themselves.

Environment Beyond the Family

Development occurs in a larger context than the nuclear family, so pubertal effects of the proximal social environment may depend on the larger environmental context. In general, family experiences extend beyond parents (e.g., peers, siblings) and are embedded in larger aspects of the environment that need to be considered in effects on development (discussed, e.g., in Bronfenbrenner & Evans, 2000).

It is particularly important to consider cultural variations. There is little information about effects on pubertal timing of specific cultural or environmental factors. In fact, a recent review (Deardorff et al., 2019) called for studying pubertal development globally, noting that variations could be driven by more than race. For example, puberty was observed to be more advanced in Black South African girls living in urban areas compared to rural areas (Cameron et al., 1993).

Sensitive Periods

There is some suggestion that experiences at ages 4–5 years might be particularly relevant for accelerating puberty (e.g., Belsky, Houts, et al., 2010; Belsky, Steinberg, et al., 2010; DiLalla et al., 2021; Ellis & Essex, 2007; Ellis et al., 1999). But there have been no explicit statistical tests of developmental effects, likely because all work relies on data from existing studies and problems of missing data in longitudinal studies. Data on developmental effects would likely help to unravel the mechanisms underlying the effects, e.g., whether cognitive capabilities developing at this age contribute to understanding the meaning or stability of supportive relationships or resources. Relatedly, it is difficult to determine if the influence of the family at one age adds uniquely to environmental influences that were already present at the preceding age. Though there is often continuity in family conditions, effects of a given environment depend on a child’s developmental stage. Children’s responses may reflect growing awareness of and sensitivity to their environments (Blair & Ursache, 2011). Separating cumulative effects from acute effects during potential sensitive periods will require longitudinal assessments. Ideally, such studies would include multiple age-appropriate measures, multiple observers/reporters, and validated continuity in the domains being studied, e.g., familial warmth.

It is also important to determine that family environment correlates of puberty are specific to the prepubertal period, by comparing how pubertal timing is linked to events experienced before versus during or after puberty; events that occur after puberty cannot contribute to its onset. Some evidence suggests that pubertal timing was associated with events occurring during puberty or later in adolescence, including father absence (Alvergne et al., 2008), and parent-child interactions (Kim et al., 1997). These reports require replication, extension to other measures, and explanation; for example, whether they reflect continuity of environmental adversity, or a third factor that influences the environment during both periods (e.g., parents’ characteristics).

Given that puberty is a series of developmental processes, it is important to incorporate development more generally into work linking early experiences to puberty. For example, it seems likely that different experiences may affect pubertal timing versus pubertal tempo; in particular, tempo may be affected by experiences that occur late in childhood, close to pubertal onset (regardless of when onset occurs), providing signals for rapid maturation. In the one study examining pubertal tempo, faster tempo before age 12.5 was associated with lower parental supportiveness (Ellis et al., 2011), but that study was not included in the table because the sexes were combined in analyses.

Child Characteristics that Modify Risk

Evidence from multiple domains shows that psychological effects of environmental experiences vary across children, with much work focusing on differential susceptibility to both positive and negative environments (e.g., Bakermans-Kranenburg & van IJzendoorn, 2015; Belsky, Bakermans-Kranenburg, et al., 2007; Belsky & Pluess, 2009). We initially planned to examine whether pubertal effects of the early family environment were moderated by the child’s sensitivity to the environment, focusing on differential responses as a function of child temperament. Unfortunately, there were few studies with sufficient data, and their results were inconsistent. Findings in one study (Belsky, Steinberg, et al., 2007) were not in line with expectation: among girls who had shown high negative emotionality in infancy (measured in an unusual way, observation during the Strange Situation), puberty was earlier if mothers were sensitive and later if mothers or fathers were harsh. Findings in another study (DiLalla et al., 2021) were also unexpected: The link between father absence and pubertal timing was not moderated by child temperament in girls, but it was in boys who experienced father absence before age 6; father absence was related to earlier pubertal timing in boys with negative affect and later pubertal timing in boys with positive affect. No other studies looked at child characteristics as a moderator of links between the early family context and pubertal timing, but such work presents a major opportunity to explain the relatively small main effects.

Sex Differences

Important questions remain about sex differences, including sex-differential effects of early environmental experiences on pubertal timing and implications for sex differences in behavior problems (male predominance in externalizing problems and female predominance in internalizing ones). Evolutionary perspectives have emphasized the trade-off between the individual’s physical development and production of offspring, with focus on girls and cursory consideration of boys. Given sex differences in the costs of reproduction, it is possible that the sexes benefit differently from environmental cues and early puberty. In particular, early maturation may be less beneficial for males than for females, given its association with smaller physical size, and the importance of size and power for dominance and status, key to male reproductive success (Wroblewski et al., 2009). Furthermore, the neuroendocrine mechanisms involved in pubertal timing may differ by sex (as occurs in nonhuman primates, reviewed by Stephens & Wallen, 2013), allowing for different influential environmental events in females versus males. This is an important area for future work, with potential implications for understanding sex differences in psychological problems given links between pubertal timing and these problems.

Specificity of Effects

It is unclear whether the experiences linked to pubertal timing are specific to those that provide signals about reproduction, the key to the hypotheses that have motivated this work (Belsky et al., 1991; Ellis, 2004). Indeed, there are no aspects of the psychosocial environment hypothesized to be unrelated to puberty or related in the opposite direction (delaying puberty). It is valuable, therefore, to investigate effects of cognitive aspects of the family environment (e.g., museum visits and puzzles not requiring positive parent-child interactions) to determine whether pubertal timing is unaffected by these types of experiences. Such studies may also shed light on whether it is the quality or quantity of adverse family environments that contribute to variations in pubertal timing.

Modifiers of Links Between Social Context and Pubertal Development

There are a number of reliable links between social context and pubertal development (e.g., exposure to adult males, parenting). But some inconsistencies need to be explored, with potential to illuminate the complexities of the links, particularly interactions among aspects of social context or between social context and other variables. As noted below, findings from nonhuman animals suggest some possibilities, including developmental stage (Hughes & Cole, 1976; Kirkwood & Hughes, 1979; Vandenbergh, 1967) and living situation (Evans & O’Doherty, 2001).

Mechanisms of Effects

Little is known about the mechanisms that mediate the effects of early environment on pubertal timing. We consider some possibilities.

Attachment

Initial hypotheses about family influences on puberty (Belsky et al., 1991) specifically focused on the role of attachment, but only one data set has been used to examine this possibility, and in a minimal way. Insecure attachment in girls was associated with earlier age at menarche and pubertal timing (both onset and completion of puberty) in one report (Belsky, Houts, et al., 2010), but not examined in another report with the same sample in which the Strange Situation was used to measure temperament (Belsky, Steinberg, et al., 2007). A hypothesized mediating mechanism of environmental effects on puberty – attachment and the mental representations formed from the early parent-child experiences – remains to be studied.

Other Psychological Processes

There has been speculation that individuals from disadvantaged backgrounds are more likely to seek immediate rewards than to delay in anticipation of better rewards (Belsky, 2012; Chisholm, 1999). For example, the well-documented link between ability to delay gratification and later success (Mischel et al., 1989) may apply primarily to well-resourced groups (Sturge-Apple et al., 2016). It is important to remember that adaptive behavioral development depends on context.

Developing cognitive capabilities may also make some age periods particularly salient for interpreting environmental events. For example, ages 4–5 represent a period of developing executive function and links between causes and effects (Blair & Ursache, 2011).

Changes in Physiology

It seems likely that environmental adversities linked to pubertal timing are biologically embedded, as are other stressors (Belsky & Shalev, 2016; Ellis, 2004; Joos et al., 2018; Zhang et al., 2019). Evidence from studies of children with extremely adverse environments (e.g., abuse) show changes to physiological systems. For example, child sexual abuse and maltreatment were hypothesized to increase physiological distress via activation and eventual dysfunction of the hypothalamic-pituitary-adrenal (HPA) and hypothalamic-pituitary-gonadal (HPG) axes, with resulting effects on pubertal development (Trickett & Putnam, 1993); links have been found between trauma and HPA dysfunction (Gunnar & Quevedo, 2008; Tarullo & Gunnar, 2006; Trickett et al., 2014), and child maltreatment, HPA function, and puberty (Negriff et al., 2015; Saxbe et al., 2015), but there has not yet been evidence for the full causal chain.

This hypothesized mechanism is supported by previous animal research. Findings suggest that early social context may influence pubertal development via changes to stressor-specific neuroendocrine pathways. Studies in pigs indicate that variations in plasma cortisol are linked to overcrowding, relocation, and exposure to boars (Hughes et al., 1990; von Borell et al., 2007). Nonhuman primate research also implicates stressor-specific mechanisms through work showing that the stress that arises from having low social rank relative to other group members may delay puberty through modification of HPA axis regulation (discussed in Ellis, 2004).

Studies in rodents document the role of parental investment in marking environmental conditions contributing to offspring reproductive behavior via epigenetic modifications as a different potential mechanism. For example, low levels of maternal care (e.g., licking, grooming) contribute to daughters’ early onset of puberty and increased mating, mediated by HPA activity and expression of estrogen receptors (discussed in Cameron, 2011). Maternal care itself is influenced by genes as well as environment (e.g., Knop et al., 2019, 2020).

Other work on mechanisms has focused on chemical signals. For example, pheromones produced by male biological family members have been suggested to inhibit early maturation (Ellis, 2004; Webster et al., 2014). Studies in rodents show how female reproductive development can be altered by exposure to same- and opposite-sex others, with puberty inhibited by members of the natal group and accelerated by exposure to unrelated males (discussed by Ellis, 2004). For example, in mice, female reproductive development can be induced by exposure to pheromones in the urine of a sexually mature (dominant) male (Vandenbergh et al., 1975).

The Role of Parents

Children’s exposure to environmental influences depends in large part on parents, who also provide genes to their children. Some influences on pubertal timing (such as family conflict and parental harshness) are both a function of parents (and thus likely to be transmitted genetically and correlated with the child’s characteristics) and an environmental context for children. Nevertheless, there has been little study of the ways that the influence of the child’s family environment reflects the characteristics of the parents. Parent personality and mental health are prime examples of the ways that parents shape children’s environment, but more work is needed to determine their roles in pubertal development, given that effects are not consistently seen. Given the relatively low rates of overt psychopathology, it is fruitful to examine effects of typical variations in personality; intriguing results suggest a link between early puberty and parental neuroticism and impulsivity (DiLalla et al., 2021).

Confounds with Genetic Influences

Relatedly, it is important to know whether family context antecedents of variations in pubertal development truly reflect environmental processes or are instead a manifestation of genetically-influenced processes (see Ellis, 2004, for related discussion). For example, a mother who had early puberty and associated behavior problems may choose a partner who has behavior problems (given assortative mating), resulting in both early divorce (father absence) and a family environment that is harsh and conflictual; the daughter would inherit genes that contribute to early puberty and an environment that is correlated with those genes. Consistent with this explanation, divorce is highly heritable, likely through genetic influences on personality (Mcgue & Lykken, 1992; Salvatore et al., 2018).

The effect of genes is best tested in an adoption study where parents’ pubertal timing, personality, and environment provided by adoptive parents are uncorrelated with characteristics of their children. Other designs can be informative, however, and the few relevant studies suggest that effects are not genetically mediated. First, controlling for mother’s age at menarche reduced but did not eliminate the link between family context and daughter’s menarche (Belsky, Houts, et al., 2010; Belsky, Steinberg, et al., 2007, 2010). It is less clear how mothers’ pubertal timing is linked to their sons’ development. Second, pubertal timing was independently predicted by polygenic risks for puberty and father absence (Gaydosh et al., 2018). Third, the link between pubertal timing and parental warmth was not due to shared genes (Rowe, 2000), but the family measures were obtained after age 7 (and thus not included in our review). Fourth, among sisters discordant for paternal dysfunction and disruption, the girls experiencing adversity had earlier puberty than those who did not, although environmental exposure was confounded with developmental status (Tither & Ellis, 2008). These studies all have their limitations, however, and this is a topic worth further exploration.

It is important to remember that pubertal development is generally under tight genetic control, given its importance to species survival, and that variations in species-typical characteristics often reflect adaptations to the environment. Thus, environmental influences on pubertal development need to be seen in the larger context of development. Puberty is not a unitary process and environmental experiences affect some aspects of puberty more than others (for review of studies in nonhuman species, see (Cameron, 2011; Ellis, 2004; Hughes, 1982; Stephens & Wallen, 2013; Vandenbergh, 1983). Evolutionary theories in particular would suggest that aspects related to reproduction are the ones that matter most, so menarche may be the aspect of puberty most sensitive to early environment. In general, studies provide more support for environmental effects on age at menarche than on other indicators of pubertal timing, but it is unclear whether that reflects measurement issues or true differential prediction. In understanding mechanisms linking early environment to puberty, it will be important to study different aspects of puberty, but this may be difficult given the need to rely on data already collected. In general, studies linking puberty to psychological development have been woefully limited in considering the multiple aspects of puberty (despite repeated calls to do otherwise; e.g., Berenbaum et al., 2015; Dorn & Biro, 2011; Mendle et al., 2019; Mendle & Koch, 2019).

Lessons from Studies in Nonhuman Animals

Our review of studies in human beings shows that pubertal timing may be altered by aspects of the early family environment. Nevertheless, the studies are limited in scope, primarily because of limitations in assessment of both puberty and behavior. It is valuable to consider how this work might be enhanced by consideration of evidence from other species. In this section, we discuss the main types of social context found to influence pubertal timing in nonhuman animals, and we consider how the work might be extended to human beings.

Comparisons between nonhuman animals and human beings need to be conditioned on cross-species differences in behavior (e.g., rodent maternal care versus parent-child interaction), living situations, reproductive strategies, and potential differential assessment, meaning, and significance of pubertal timing. For example, early puberty may be advantageous to one species but disadvantageous to another; puberty in nonhuman animals is generally conceptualized as reproductive readiness rather than pubertal timing. Variations across species may also be due to species-specific characteristics; for example, social species are more likely to be influenced by social context than are nonsocial or solitary ones. Furthermore, different methods are used in different species, particularly laboratory versus field studies.

Nevertheless, studies in nonhuman animals have considerable potential to inform future work on pubertal timing in human beings. Given the findings described below, we summarize in Figure 2 proposed parallels between social context across species, with suggestions for ways to extend human research on the antecedents of pubertal timing.

Proposed Parallels Between Animal and Human Social Environment in Review

*Note*. Social context characteristics shown in the left column have been found to be associated with pubertal timing in nonhuman species. Social context characteristics shown in the right column are suggested to provide parallels to factors in the same row and to influence human pubertal timing.

Exposure to Adult Males

Puberty is accelerated by exposure to adult males in female rodents (Carter et al., 1980; Drickamer & Murphy, 1978; Hasler & Banks, 1968; Vandenbergh, 1967, 1969, 1976; Vandenbergh et al., 1972), pigs (Brooks & Cole, 1970; Hughes, 1994; Mavrogenis & Robison, 1976; Thompson & Savage, 1978), cotton-top tamarins (Ziegler et al., 1987), cows (Izard & Vandenbergh, 1982), goats (Amoah & Bryant, 1984), and red deer (Fisher et al., 1995). Findings across these species indicate that exposure to adult males occurring any time before puberty can accelerate puberty, but exposure during the prepubertal stage has a stronger effect on pubertal timing than exposure during infancy, at least in rodents (Vandenbergh, 1967) and pigs (Hughes & Cole, 1976; Kirkwood & Hughes, 1979). These effects parallel those in girls showing that stepfather presence (Ellis & Garber, 2000; Steppan et al., 2019) and biological father absence (Table 1) accelerate pubertal timing.

Other Aspects of Family Composition

Composition of the family/group is related to pubertal timing in both female and male animals. Puberty in female rodents was seen to be delayed by exposure to unrelated adult females at any time prior to puberty (Coppola & Vandenbergh, 1985; Cowley & Wise, 1972; McIntosh & Drickamer, 1977). Female common marmosets’ puberty was delayed by exposure to mothers (Abbott, 1984; Evans & Hodges, 1984; Saltzman et al., 1997). Earlier age of menarche in female baboons was linked to more maternal half-sisters present when menarche occurred (Charpentier et al., 2008). In male baboons, accelerated puberty was associated with excess females present when puberty began (Charpentier et al., 2008). Similar effects have been observed in human beings: Menarche was delayed in girls with older sisters (Bogaert, 2008; Matchock & Susman, 2006); girls who lived with half- and step-siblings had earlier pubertal timing than girls who lived with only full biological siblings (Lenárt et al., 2019; Matchock & Susman, 2006; Smith, 2017), but findings could have been confounded with the presence of unrelated adult males such as stepfathers.

Small group size was associated with earlier puberty in female baboons (Charpentier et al., 2008). This has a parallel in human beings: Larger family size (e.g., number of siblings) has been related to later pubertal timing in girls (Azcorra et al., 2018; Billewicz et al., 1981; Dann & Roberts, 1993; Krzyżanowska et al., 2016; Malina et al., 1997; Morris et al., 2010; Ossa et al., 2010; Padez, 2003; Rigon et al., 2010; Sánchez-Andrés, 1997; Sheppard et al., 2014, 2015; Szwed et al., 2013), and perhaps in boys (Sheppard et al., 2015).

Population Density

Population density has been related to variations in pubertal timing in animals, but the nature of its effect is not consistent. Higher density during the juvenile period (any time between infancy and puberty) has been associated with earlier pubertal timing in both female and male pigs (Mavrogenis & Robison, 1976; Thomas et al., 1979) and later pubertal timing in female mice (Coppola & Vandenbergh, 1985; Drickamer, 1974). Population density may be similar to SES-related physical environment in humans, but, as noted above, SES indexes a variety of physical and social factors.

Maternal Care

Female pubertal timing in rodents is accelerated by low maternal care, particularly licking and grooming, during infancy (Cameron et al., 2008). These maternal behaviors may parallel human parenting and childcare, and subsequent family environment quality discussed above.

Social Rank

High juvenile social rank within the community is related to early pubertal timing in both males and females in primates (Alberts & Altmann, 1995; Bercovitch et al., 1993; Charpentier et al., 2008; Schwartz et al., 1985; Wilson et al., 2013; Zehr et al., 2005). Human parallels to social rank within the community may include communal living, peer social rank, and SES (although, as discussed above, SES is heterogeneous and therefore inconsistently related to pubertal timing). Peer social rank that can be observed through peer interactions, such as bullying, dominance status within friendship networks, and degree of social isolation, has yet to be investigated with respect to pubertal timing.

Psychological, Physical, and Reproductive Health Significance of Effects

Links between early family environment and pubertal timing are small to moderate (not surprising, in light of the high heritability of puberty; Corley et al., 2015; Eaves et al., 2004; Pham et al., 2021; van den Berg et al., 2006), but they are meaningful – and effects might be larger in some contexts and for some children. Effects of this magnitude are similar to effects in other areas of child development, and such effects likely have consequences, particularly for public health. For example, the typical correlation of 0.2 translates to two months advancement in menarche for a standard deviation increase on a measure of harsh home environment.

Parental effects on girls’ pubertal timing also compare favorably to the small-to-medium effects of early parenting on other measures. These effects include both physiology, such as skin conductance reactivity (Erath et al., 2009) and stress reactivity (Sturge-Apple et al., 2012), and behavior, such as internalizing and externalizing problems (reviewed in Hoskins, 2014).

Pubertal timing continues to have effects beyond adolescence, as seen in adult psychological and physical health. Pubertal timing’s link to depression continues into adulthood (Graber, 2013; Negriff & Susman, 2011). With respect to physical health, pubertal timing has both positive and negative effects (Daniel & Balog, 2009; Karapanou & Papadimitriou, 2010). In men, adult fracture risk was increased 5% for every year increase in pubertal timing (Vandenput et al., 2019). In women, different risks have been associated with early versus late menarche (Mishra et al., 2009). For example, meta-analysis revealed that breast cancer risk decreased by 5% for every year menarche was delayed (Collaborative Group on Hormonal Factors in Breast Cancer, 2012), and one large epidemiological study showed that dementia risk increased by 23% for women who had late menarche (after 16 years of age) (Gilsanz et al., 2019).

Social context effects have been well-studied with respect to human behavior (e.g., Colich et al., 2020; Smith et al., 2013), and they are increasingly recognized to affect human puberty. Furthermore, pubertal development itself is tied to various aspects of human behavior such as psychopathology (reviewed in Graber, 2013; Hamlat et al., 2019; Negriff & Susman, 2011; Ullsperger & Nikolas, 2017). Animal studies make clear that social context influences on some behaviors are related to their effects on reproduction. For example, maternal care is linked to offspring’s own quality of maternal care in rodents (Cameron, 2011), and to many aspects of reproductive functioning, including sexual behavior, fertility, timing of first birth, and lifetime reproductive success (Cameron et al., 2008), and pubertal development appears to mediate the links between social environment and outcomes (Cameron, 2011; Romeo, 2003).

It is clear that variations in pubertal timing have long-term implications for health. Understanding early predictors of puberty may suggest potential intervention targets and thus contribute to improving health.

Conclusions

Findings across a range of studies suggest that girls growing up in typical families may have their pubertal timing altered by variations in their family environment. Effects are generally small in size, not surprising given the biological significance and high heritability of puberty, but they are comparable to other effects on development, and have implications for health.

The dearth of data in boys prevents any conclusions about environmental influences on their pubertal timing, and this issue clearly requires attention. Recent work has highlighted the gap in understanding pubertal development in boys and its impact on psychological health (Deardorff et al., 2019; Mendle et al., 2019).

Our review was novel in highlighting findings, identifying opportunities regarding the impact of family environment on pubertal timing, and linking human research to work with nonhuman species. We also note caveats that reflect the limitations of the studies we reviewed, particularly the conceptualization and measurement of both pubertal timing and family environment, considerable reliance on retrospective data, and concerns about missing data.

Much remains to be understood about the nature, mechanism, and meaning of links between early family environment and puberty in human beings – and this presents clear opportunities for future work. In particular, it is important to understand what aspects of the environment are most important for what aspects of puberty, whether environments matter across the range of exposures, how parents themselves create risk or protection beyond the parenting behaviors that are typically studied, and what factors modify the effects on puberty of family environment, including the child’s sex and sensitivity to the environment, the age at which the experiences occurred, and the broader social context. Providing this missing information should help to delineate the hormonal mechanisms that underlie environmental effects on puberty and behavior. They also have the potential to contribute to understanding basic developmental processes and enhancing public health. Future work focused on these questions should be interdisciplinary, drawing on foundational findings from animal studies and expertise in the biology of pubertal development, developmental sciences, and family and peer functioning (Susman et al., 2019). Work in nonhuman animals can help to guide human research in human beings, and attention to cross-species parallels will be critical in moving the field forward.

Highlights.

Negative family context is linked to earlier pubertal timing in girls
It is still unclear if boys’ pubertal timing is influenced by family context
Current conceptual and methodological challenges impact interpretations of findings
Many research opportunities on psychosocial influences on pubertal timing exist
Social environment-puberty links in people may parallel links in other species

Acknowledgments

This work was supported by the National Institutes of Health under R01 AG046938.

Footnotes

We have no conflicts of interest to disclose.

Google Scholar, PsycINFO, and Web of Science databases were used to search for empirical papers published in April 2021 or earlier using the following search terms: early life, parent/father absence, family/marital/home/parent conflict, divorce, family disruption, family/parental approval/warmth/sensitivity/supportiveness/closeness/cohesion/expressiveness, harsh parenting/parental harsh control/discipline, family life stress/adversity, family relationships/relationship quality, parent psychopathology, parent personality, marital stress/satisfaction, parent emotional tone/affect, age at menarche, puberty, pubertal timing, pubertal development, life history theory, reproductive development/strategy

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PERMALINK

Family Environmental Antecedents of Pubertal Timing in Girls and Boys: A Review and Open Questions

Holly T Pham

Lisabeth F DiLalla

Robin P Corley

Lorah D Dorn

Sheri A Berenbaum

Abstract

How Do Typical Variations in the Early Family Context Affect Pubertal Development?

Evaluating Early Family Context Effects on Pubertal Timing

Table 1.

Focus of the Review

Figure 1.

Criteria for Inclusion

Interpreting Results

Evidence for Early Family Context Effects on Pubertal Development

Effect Size

Type of Early Family Context

Parents’ Characteristics

Developmental Effects

Sex Differences

Conceptual and Methodological Issues in Evaluating Studies

Assessment of Puberty

Assessment of Features of Family Context

Open Questions and Opportunities for Research

Practical Challenges and Solutions

Availability of Prospective Data

Sample Recruitment and Retention

Inclusion of Boys

Determining the Nature of the Effects

The Meaning of Father Absence

The Form of the Association

Positive vs. Negative Experiences

Accumulation of Adverse Experiences

Environment Beyond the Family

Sensitive Periods

Child Characteristics that Modify Risk

Sex Differences

Specificity of Effects

Modifiers of Links Between Social Context and Pubertal Development

Mechanisms of Effects

Attachment

Other Psychological Processes

Changes in Physiology

The Role of Parents

Confounds with Genetic Influences

Lessons from Studies in Nonhuman Animals

Figure 2.

Exposure to Adult Males

Other Aspects of Family Composition

Population Density

Maternal Care

Social Rank

Psychological, Physical, and Reproductive Health Significance of Effects

Conclusions

Highlights.

Acknowledgments

Footnotes

References

ACTIONS

PERMALINK

RESOURCES

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