Why are girls and boys maturing earlier?

For girls, the age of puberty has been falling since the 19th century. The same period has seen a similar decline for boys (source)

In the United States and other Western countries, girls have been reaching puberty at earlier and earlier ages. A recent longitudinal study has examined this trend in white Americans born between 1928 and 1992. Its conclusion? Girls are reaching puberty earlier because of an interaction between a lifestyle factor and a pre-existing genetic predisposition:

Our data also show, for the first time, that the effect of menarche SNPs on prepubertal BMI was stronger in children born more recently compared to those born earlier in the century, thereby suggesting that the developmental genetic susceptibility to elevated BMI may have only been ''uncovered'' in the more obesogenic environments of the recent past. (Johnson et al., 2013)

For the study's authors, the lifestyle factor is that girls are eating more, exercising less, and accumulating more body fat. Because fatty tissue is a significant source of estrogen, an increasing percentage of body fat tends to hasten puberty in young girls (Frisch & Revelle, 1970; Frisch & McArthur, 1974; Kaplowitz et al., 2001; Siiteri & MacDonald, 1973). This effect is stronger in girls with a certain genetic background:

It is possible that over the examined time period, individuals with higher genetic burden for accelerated sexual development are for the first time ''allowed'' by liberalization of the environment to alter dietary intake and energy expenditure to support their genetic potential for rapid weight gain and earlier sexual development. (Johnson et al., 2013)

But why are boys too maturing earlier?

In boys, body fat is not linked to early puberty. In fact, there seems to be a negative correlation, perhaps because fatty tissue is a significant source of estrogen (Wang, 2002). Overweight boys often present signs of disrupted male sexual development, e.g., breast budding, higher voice pitch, etc.

Yet boys likewise are reaching puberty at an earlier age. This is the conclusion of a recent American study:

We observed that onset of secondary sexual characteristics in US boys as seen in office practice appears to occur earlier than in previous US studies and the 1969 British study commonly used for pubertal norms. […] White boys in our study entered stage 2 genital growth 1.5 years earlier than the British boys (10.14 vs 11.60 years of age).

[…] These data are consistent with recent trends from other countries, such as Denmark, Sweden, Great Britain, Italy, and China. For example, urban Han Chinese boys achieve a testicular volume of ≥4 mL (13% by age 9) and spermarche earlier than studies conducted several decades ago; Danish boys achieve a testicular volume >3 mL more than 3 months earlier now than 15 years ago. (Herman-Giddens, 2012)

This trend has also been observed in the age when a boy's voice begins to change:

According to records kept by the Leipzig choir, the most common period of voice breaking for male singers in the mid-18th century was between 17.5 and 18.5 years of age (Daw, 1970); in contrast, children enrolled in the Copenhagen Municipal Choir School from 1994-2003 had a median age of voice breaking of 10.4 years (Juul, Magnusdottir, Scheike, Prytz, & Skakkebæk, 2007), which is consistent with the choir's subjective reports of difficulty retaining children as singers past the age of 12 or 13 years. (Mendle & Ferrero, 2012).

This is a challenge for Occam's Razor, and the task is no easier if we look at other possible causes. If the cause isn’t a higher proportion of body fat, could it be a higher level of estrogens and estrogen-like substances in the environment? (see earlier post). Yes, that might hasten puberty in girls and increase accumulation of body fat. But in boys it would delay puberty by offsetting the rising level of male hormones.

In trying to figure out the causal chain of events, we should keep in mind that the relationship between body fat and age of puberty runs in both directions. On the one hand, estrogen from body fat lowers the age of puberty in girls. On the other hand, earlier puberty increases ovarian production of estrogen, which in turn stimulates deposition of body fat, particularly on the hips, buttocks, and breasts (Van Lenthe et al., 1996). So perhaps some unknown factor is causing earlier sexual development in both sexes and thus greater deposition of body fat in girls.

A response to social cues?

This unknown factor might be something in the social environment. As Hawley (2011) argues, humans unconsciously monitor their social environment for reproductive opportunities and accordingly speed up or slow down their pace of sexual development:

[...] human children, especially girls, may be sensitive to their early socioecological conditions in ways that entrain development toward either a faster (earlier pubertal maturation, more sexual partners, less stable relationships) or slower (later pubertal maturation, fewer sexual partners, more stable relationships) life history strategy.

With the transition to post-traditional societies, there has been an increase in the erotic stimuli that preteens encounter in their surroundings:

Common in traditional societies are adult-supervised adolescent initiation ceremonies (Schlegel & Barry, 1980) that are designed to commemorate the transition from childhood to adulthood and inculcate the adolescent with adult values, duties, behaviors, and sex roles associated with the culture (Schlegel, 1973). That is, these adolescents are taught adult sex roles by adults. We now appear to have a complete turnaround. In modern, Western cultures, adolescents derive sexual relationship expectations from television, cable, music, purveyors of racy lingerie (who target teenage girls), and pornography that they can now access on the Internet and thereby carry around on their cell phones. (Hawley, 2011)

Erotic imagery in particular is today available to a degree that was impossible not so long ago. Young boys and girls have virtual access to an endless supply of picture-perfect sexual partners. Whatever the media—films, TV, magazines, the Internet—we're exposed to images that can stimulate sexual desire as efficiently as what normally exists in the real world. More so, in fact. These images are ‘supernormal’ stimuli.

To date, only one study has looked into possible relationships between erotic imagery and pubertal timing:

The aim of this study was to investigate associations between pubertal timing and boys' Internet use, particularly their viewing of pornography. We used a sample comprising of 97 boys in grade 8 (M age, 14.22 years) from two schools in a medium-sized Swedish town. This age should be optimal for differentiating early, on-time, and later-maturing boys. Boys responded to self-report questionnaires on their Internet use and pubertal timing. Early, on-time, and late-maturing boys did not differ in terms of most Internet activities. However, early maturers reported downloading and viewing pornography more often than the other boys did (p<.001). (Skoog et al.,2009)

Admittedly, the arrow of causality might point in the other direction, i.e., early maturing boys have a stronger sex drive and thus a greater interest in porn. This was, in fact, the authors' explanation. We should also remember the well established correlation between early puberty in girls and the absence of a father in the home. It was long thought that father absence triggers early puberty in girls. In fact, a twin study has shown a genetic cause: absent fathers tend to have genes that favor earlier sexual development in their progeny (Mendle et al., 2006).

One might also object that the decline in the age of puberty began long before the Internet. Before the Internet, however, there were porn magazines. And before them, there were pictures garnered from art books, fashion magazines, or the lingerie sections of mail-order catalogues. One could also bring erotic images to mind by reading certain novels. Thus, modern pornography is merely the latest stage of a lengthy co-evolution between, on the one hand, improvements in photography and other imaging technologies and, on the other hand, a weakening of taboos against masturbation. At the beginning of this co-evolution, in the 19th century, masturbation was much less developed among young boys and girls as a sexual lifestyle. Visual aids were scarce and of poor quality, religious injunctions were strong, and adult supervision inside and outside the home was omnipresent.

Conclusion

The age of puberty might be declining because boys and girls are being exposed to ever more and ever better erotic imagery, but this hypothesis needs confirmation by longitudinal studies to determine which is the cause and which is the effect. Another drawback with current research is its focus on the most extreme forms of pornography, such as child porn. Yet the usual stuff is the kind that most people consume ... and in unparalleled quantities. As the authors of a recent Dutch study remarked:

[...] we can only emphasize that Dutch youth are confronted with and expose themselves to an unprecedented amount of R-rated and Xrated material in the media. Research on its consequences for adolescents' sexual socialization is largely missing but, as this study has shown, is urgently needed. (Peter & Valkenberg, 2006)

And erotic imagery isn't confined to X-rated websites or magazines. It is in fact ubiquitous in modern social environments. Girls might accelerate their sexual development by leafing through fashion magazines just as boys might accelerate theirs by viewing porn.

The erotic imagery hypothesis will have to fit the data better than rival hypotheses. Two of these, the body fat and environmental estrogen hypotheses, can explain the decline in the age of puberty for girls but not for boys. Another possible cause is better nutrition. Yet, among white Americans at least, much of this decline has happened since the 1950s—when nutrient levels were already adequate for this population. Finally, there is the possibility that puberty is happening earlier because genes that favor that developmental trajectory are spreading within the population. Modern social environments favor a reproductive strategy of early puberty, low parental investment and, especially, low paternal investment—in short, the ‘cads’ are outbreeding the ‘dads’ (see earlier post).

References

Frisch, R.E., R. Revelle. (1970). Height and weight at menarche and a hypothesis of critical body weights and adolescent events, Science, 169, 397-399.

Frisch, R.E. & J.W. McArthur. (1974). Menstrual cycles: fatness as a determinant of minimum weight necessary for maintenance or onset, Science, 185, 949-951.

Hawley, P.H. (2011). The evolution of adolescence and the adolescence of evolution: The coming of age of humans and the theory about the forces that made them, Journal of Research on Adolescence, 21, 307-316.

http://www.people.ku.edu/~phawley/Publications/Hawley%202011%20JRA%20Evo%20of%20Adol.pdf

Herman-Giddens, M.E., J. Steffes, D. Harris, E. Slora, M. Hussey, S.A. Dowshen, R. Wasserman, J.R. Serwint, L. Smitherman, & E.O. Reiter. (2012). Secondary sexual characteristics in boys: Data from the Pediatric Research in Office Settings Network, Pediatrics, 130, e1058-e1068.

http://pediatrics.aappublications.org/content/130/5/e1058.full.pdf+html

Johnson, W., A.C. Choh, J.E. Curran, S.A. Czerwinski, C. Bellis, T.D. Dyer, J. Blangero, B. Towne, & E.W. Demerath. (2013). Genetic risk for earlier menarche also influences peripubertal body mass index, American Journal of Physical Anthropology, 150, 10-20

Kaplowitz, P.B., E.J. Slora, R.C. Wasserman, S.E. Pedlow & M.E. Herman-Giddens. (2001). Earlier onset of puberty in girls: relation to increased body mass index and race, Pediatrics, 108, 347-353.

Mendle, J. & J. Ferrero. (2012). Detrimental psychological outcomes associated with pubertal timing in adolescent boys, Developmental Review, 32, 49-66.

Mendle, J., E. Turkheimer, B.M. D'Onofrio, S.K. Lynch, R.E. Emery, W.S. Slutske, N.G. Martin. (2006). Family structure and age at menarche: a children-of-twins approach, Developmental Psycholpgy, 42, 533-542.

Peter, J. & P.M. Valkenberg. (2006). Adolescents' exposure to sexually explicit material on the Internet, Communication Research, 33, 178-204.

Siiteri, P.K. & P.C. MacDonald. (1973). Role of extraglandular estrogen in human endocrinology. In S.R. Geiger (ed.), Handbook of Physiology, Washington D.C. American Physiology Society, sect. 7, vol. 2, part 1, pp. 615-629.

Skoog, T., H. Stattin, & M. Kerr. (2009). The role of pubertal timing in what adolescent boys do online, Journal of Research on Adolescence, 19, 1-7.

Van Lenthe, F.J., C.G. Kemper & W. van Mechelen. (1996). Rapid maturation in adolescence results in greater obesity in adulthood: the Amsterdam Growth and Health Study, American Journal of Clinical Nutrition, 64, 18-24.

Wang, Y. (2002).Is obesity associated with early sexual maturation? A comparison of the association in American boys versus girls, Pediatrics, 110, 903-910.

http://www.pediatricsdigest.mobi/content/110/5/903.short

Bringing reproductive maturity into line with the age of marriage

Île aux Coudres, a French Canadian community on an island in the St. Lawrence

Human biodiversity is slowly making headway in academia. It has three defining principles:

1. Evolution did not end, or even slow down, with the advent of Homo sapiens. It has actually accelerated.

2. It especially accelerated about 10,000 years ago, when the rate of genetic change rose over a hundred-fold among early modern humans. This acceleration didn’t happen because they were spreading into new physical environments with different climates, topographies, vegetation, and wildlife. By then, humans had already spread throughout the world from the equator to the arctic. They were now spreading into new cultural environments with different technologies, social structures, belief systems, and means of subsistence.

3. The human species has therefore experienced more genetic change over the past 10,000 years than over the previous million years. This change has particularly involved genes for mental, behavioral, and life-history traits (Frost, 2011; Hawks et al., 2007).

One life-history trait is the age of first reproduction (AFR). Because AFR is highly heritable, there may have been co-evolution between biology and culture. In other words, natural selection has tended to bring full reproductive maturity into line with the age when young couples have enough resources to marry and start a family.

When Europeans first began to settle North America, they came from a land-poor environment where young people had to postpone marriage and family formation. Typically, they had to wait until their parents handed over the farm in whole or in part. This tendency toward late marriage was widespread throughout Western Europe, so much so that it has been dubbed the ‘Western European Marriage Pattern’:

[…] the late and non-universal marriage pattern was definitely prevalent across Northwestern Europe in the seventeenth century. By 1650, when village reconstitution studies become sufficiently numerous to render the generality of the pattern indubitable, the average age of women at first marriage was twenty-four or over, 7 to 20 per cent of women never married, and the incidence of childbirth out of wedlock was below 3 per cent. This marital pattern restricted fertility massively. A very considerable minority of women remained single and bore no children; those who married bore none for the first ten years of their fecund life-phase, on average. If they had their last child at the age of forty, their entire reproductive careers would span roughly fifteen years, a long time by modern standards but remarkably brief in a pre-transition context. Resulting fertility was less than half the rate that would have been achieved if all women between fifteen and fifty were married. (Seccombe, 1992, p. 184)

All of this changed when Europeans began to settle in the “New World.” Suddenly, land was no longer a constraint on marriage, and early marriage became the norm. With the downward shift in the age of marriage, was there a corresponding downward shift, via natural selection, in the age of full reproductive maturity?

Yes, according to a recent study of Île aux Coudres, a French Canadian community on an island in the St. Lawrence. Over a period of 140 years, from 1800 to 1940, this community saw its mean AFR fall by four years. This decline was driven not by a lowering of the mean age of marriage (which now remained stable) but by a shortening of the mean interval between marriage and first birth.

The decline in AFR seems to have been real, and not an artefact of incomplete marriage and birth records. In fact, the church registers provide exceptionally detailed birth and marriage data. Nor was it an artefact of an influx of people with lower AFRs. Almost everyone on Île aux Coudres is descended from thirty families who settled the island between 1720 and 1773.

Could the reason have been changes to diet and nutrition? Unlikely.

The advancement of age at maturity, as well as increases in fertility, may reflect plastic responses to improvements in nutritional conditions, such as those observed during the 19th and 20th centuries in Western societies. Better-fed women grow faster, mature earlier and in a better physiological state, and are more fecund. Importantly, alongside such plastic responses in reproductive traits, we would expect an increase in infant and juvenile survival rates with time. Despite some fluctuations, infant and juvenile survival rates on île aux Coudres were not higher at the end of the study period than at the beginning. (Milot et al., 2011)

When I first heard of this study, I thought that some kind of cultural lag might have been responsible. Old habits die hard. Perhaps many of the early settlers, with memories of the old country, were still afraid of not having enough land to support a family, even after they had decided to marry. This reticence would have then gradually disappeared as memories of the old country disappeared.

Such a change in mentality, however, would have happened much more among the earlier generations than among the later ones. Yet this is not what we see in the data. AFR changed at the same rate from one generation to the next throughout the 140-year period. Couples married after 1870 showed the same rate of change as couples married before 1870. Indeed, this steady rate of change seems to rule out most socio-cultural explanations, particularly those that involve some kind of re-adjustment to new conditions. In any case, the study period (1800 to 1940) postdates the years of immigration and settlement (1720 to 1773).

We’re certainly going to see more studies like this one, either from Île aux Coudres or from other regions of French Canada. In general, French Canadian communities are ideal for the study of human microevolution. Records of births, marriages, and deaths are remarkably complete over a span of three centuries, and the inhabitants tended to stay put in the same locality generation after generation. For several regions of Quebec, we already have complete genealogical databases that could be enriched with genetic data for the most recent generations.

Reference

Frost, P. (2011). Human nature or human natures? Futures, 43, 740-748. http://dx.doi.org/10.1016/j.futures.2011.05.017

Hawks, J., E.T. Wang, G.M. Cochran, H.C. Harpending, & R.K. Moyzis. (2007). Recent acceleration of human adaptive evolution, Proceedings of the National Academy of Sciences (USA), 104, 20753-20758.

Milot, E., F.M. Mayer, D.H. Nussey, M. Boisvert, F. Pelletier, and D. Réale. (2011). Evidence for evolution in response to natural selection in a contemporary human population, Proceedings of the National Academy of Sciences (USA), early view

Seccombe, W. (1992). A Millennium of Family Change. Feudalism to Capitalism in Northwestern Europe, London: Verso.

More on father absence

I used to believe in a direct causal link between father absence and early sexual maturity in girls. The reasoning was that a daughter’s sexual development is accelerated when her biological father is replaced by a strange male (such as a stepfather). At the time, I saw this finding as a way to counter the argument that sociobiology denies human plasticity. It also offered hope that we could remedy a large number of social problems by ensuring father presence. Now I can’t help wondering whether all of this distorted my sense of judgment … and that of others.

One of the best studies on this subject is by Surbey (1990), who used a large sample (1,247 daughters) and measured several possible confounding factors: family size, birth order, weight, height, Quetelet Index, and socio-economic status (SES). On none of these measures did the father-absent daughters (16% of the sample) significantly differ from the father-present daughters. Nonetheless, they matured 4-5 months earlier than those who lived with both parents continuously and 7 months earlier than those who had experienced only an absent mother.

That sounds convincing. Yet how well was SES really controlled? The subjects were apparently university students, so they would have shared the SES of their mothers. But what about the SES of their absent fathers? What do we know about them? Typically nothing. And does SES fully capture all of the factors that distinguish father-absent daughters from father-present ones? Could it be that these two groups differ somewhat in their physiological make-up and, perhaps, in their genetic background?

These doubts led Mendle et al. (2006) to control for genetic background by examining the daughters of twin mothers. It turned out that the daughters did not differ in age of menarche if one mother was still living with the biological father and the other was not. Moreover, when the mother’s age of menarche was controlled among unrelated daughters, age of menarche no longer differed between daughters living with stepfathers and those living with biological fathers.

The presence of a step-uncle was as strongly predictive of early menarche as presence of a stepfather. It does not seem necessary for a child to experience the direct environmental influence of a stepfather to exhibit an accelerated age of menarche—as long as she is genetically related to someone who does have a stepfather. In a pair of twin mothers of which only one raises her children with a stepfather, the offspring of both twins are equally likely to display early age of menarche. It therefore appears that some genetic or shared environmental confound accounts for the earlier association found in female children living with stepfathers.

Mendle et al. (2006) raised another point. The correlation between father-absence and early menarche may be an artefact of population substructure:

The wholly Caucasian population of our Australian sample may explain our failure to replicate the strong father-absence association observed in more ethnically diverse American samples. Given that African American and Latina girls experience menarche on average 6 months prior to Caucasians (Herman-Giddens et al., 1997), it may be that the previously established associations between early menarche and lack of a traditional two-parent family structure are affected by racial differences in family structure. Correlates of early menarche may additionally be complicated by effects of poverty or socioeconomic status. For example, Obeidallah, Brennan, Brooks-Gunn, Kindlon, and Earls (2000) obtained a difference in age of menarche between Caucasian and Latina girls, but this effect disappeared after controlling for socio-economic status.

Why didn’t other studies control for ethnicity? Apparently because the authors felt that SES controls were sufficient. This may be true for Hispanic Americans but it is not for African Americans. Even among Hispanics, there may still be substructure effects. It is known that Hispanic SES correlates with European ancestry, so controlling for SES would bias this population toward individuals who are more genetically similar to European Americans.

All of this makes me wonder about all of the data that supposedly prove the adverse effects of single motherhood. Undoubtedly, there are adverse effects. But there are probably many “pseudo-effects” that would persist even if the biological father could be forced to stay around.

For what it’s worth, I spent part of my pre-adult life in a father-absent family (my father died of a cerebral hemorrhage). Yes, there were adverse effects, poverty in particular. Nonetheless, I think I would have ended up being substantially the same kind of person even if my father had continued to live.

References

Mendle, J., Turkheimer, E., D’Onofrio, B.M., Lynch, S.K., Emery, R.E., Slutske, W.S., Martin, N.G. (2006). Family structure and age at menarche: a children-of-twins approach. Developmental Psychology, 42, 533-542.

Nettle, D. (2008). Why do some dads get more involved than others? Evidence from a large British cohort. Evolution and Human Behavior, 29, 416-423.

Surbey, M.K. (1990). Family composition, stress, and the timing of human menarche. In T.E. Ziegler & F.B. Bercovitch (eds.) Socioendocrinology of Primate Reproduction, pp. 11-32, New York: Wiley-Liss Inc.