Trends in Endocrinology & Metabolism
Evolution, development and timing of puberty
Introduction
There is considerable public and medical interest in the falling age of menarche [1]. This reflects an increasing awareness of the consequences of the psychosocial ‘mismatch’ which arises from early biological reproductive competence in societies in which young women do not obtain psychological or social maturity until at least their late teens [2]. Precocious puberty might be a result of identifiable central or peripheral pathology (Box 1). Most cases of central precious puberty are ‘idiopathic’, and within this group of children are many in which the progression of puberty is unremarkable other than being somewhat earlier in onset.
Particular attention has focused on an apparently greater incidence of early-onset puberty in girls who migrated at a young age from a poor to a developed country [1]. One explanation is that this phenomenon results from greater environmental exposure to developmental endocrine disruptors, such as derivatives of dichloro-diphenyl-trichloroethane, thus accelerating hypothalamic maturation [1]. Such considerations imply a pathological origin. Generally, a medical approach is taken to early menarche. The use of suppressors of gonadotrophin secretion or action has increased. For example, there is an increased use of such agents in association with growth hormone therapy for impaired skeletal growth, although the evidence for auxological efficacy is debatable 3, 4. A more parsimonious explanation for both the secular trend and the observations made in the migrant population is that these are reflections of the underlying evolved life history strategies of Homo sapiens.
Here, we review evidence suggesting that the timing of puberty and its other characteristics can be better understood by reference to evolutionary principles. These considerations place early-onset menarche in perspective, challenge the concept that it is necessarily pathological and suggest a need for a greater societal awareness of the biological inevitability of early menarche in the 21st century. Although many similar considerations might apply to males, the reproductive and life history strategies of the two genders are quite distinct and this might be reflected in the more frequent presentation of females with early-onset puberty. Further, the absence of an easily assessable marker of potential reproductive competence means that discussion will focus on the female.
Section snippets
Life history, reproductive competence and puberty
The attainment of reproductive competence is central to the life history of all sexually reproducing organisms. In mammals, this manifests as puberty. Natural selection favours individuals who optimize their capacity to pass their genes to the next generation. Reproductive fitness is enhanced if there is an adaptive match between the life history traits of the organism and the environment in which it has evolved to live. Key traits include the pattern of growth, timing of growth phases, optimal
Genetic influences on the timing of puberty
About half the variance in the timing of menarche is genetically determined [8], and there is evidence for a dominant inheritance pattern [9]. Several polymorphisms including shorter TAAAA repeats in the promoter region of the gene for the sex hormone binding globulin [10], and single nucleotide polymorphisms in CYP17 11, 12 and CYP3A4 [13] have been implicated. Evidence for genetic effects on the timing of puberty can also be inferred from the secular trend in the age of menarche. Northern
Environmental influences on the timing of menarche
Life history theory suggests that nutritional influences, both in early development and in childhood, would have significant effects on the timing of puberty [18]. In epidemiological studies, a common finding is a trend towards earlier menarche in those of lower birth weight or low body mass 19, 20, 21, 22, 23. As the timing of adrenarche appears to be similarly influenced [24], it suggests a general effect on maturation rather than a specific effect on the hypothalamic gonadostat [25]. This
The interaction between prenatal and postnatal influences
These two developmental effects become manifest most dramatically in the combination of prenatal early life deprivation with childhood nutritional excess, as seen in adopted children migrated from poor to rich countries 1, 38. Both environmental effects are predicted to advance menarche. We anticipate that the prenatal effect would be stronger in those children born small who are in a nutritionally enriched postnatal environment, as reflected in good weight gain in childhood, and indeed this is
The secular trend in menarche and the mismatch produced
There is a consensus that in developed countries there has been a marked secular trend for a reduction in the age of menarche over the past 100 years 1, 14, 15, 16, 17. In populations of Northern European origin, the age of menarche is approximately three years earlier than it was 100 years ago 1, 40. Similar but less dramatic trends can be observed in other populations. This trend is generally interpreted as being a reflection of improved nutrition and reduced infection in childhood over the
The pubertal growth spurt
Another unique feature of humans is the pubertal growth spurt, there being no evidence of such spurts in skeletal dimensions in other primates. Most mammals undergo puberty as their postnatal growth is tailing off [42]. In humans, reproductive competence is achieved early in the growth spurt in males and at a later stage in females [25] but in both genders it is underpinned by oestradiol. Although there is a small amount of linear growth after menarche, most cycles in the first year after
Final comments
We have suggested that an evolutionary perspective is useful in understanding various components of contemporary human puberty. This perspective argues for more careful use of the term ‘precocious puberty’. This term implies pathology and, although there are important organic causes of central and gonadal precocious puberty and onset of puberty at a particularly young age is clearly pathological, the vast majority of young women undergoing menarche at increasingly younger ages have normal
Acknowledgements
We thank Patrick Bateson, Barry Bogin, Peter Ellison, Marta Lahr, Rob Foley and Wayne Cutfield for valuable discussions.
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