Rapid weight gain after birth predicts life history and reproductive strategy in Filipino males

Abstract

Ecological cues during prenatal and postnatal development may allow organisms to adjust reproductive strategy. The hypothalamicpituitary-gonadal (HPG) axis is a prime candidate for adaptive plasticity as a result of its critical period of birth to 6 mo (B6M) in humans and the role of testosterone in the development and maintenance of costly sexually dimorphic somatic and behavioral traits. We hypothesized that weight velocity specific to B6M would predict male life history characteristics, including maturational timing, reproductive hormones, adult size, strength, and sexual activity. Data come from 770 Filipino men (age 20.5-22.5 y) followed since birth, with predictor variables including birth weight and weight velocities calculated at 6-mo intervals during the first 2 y of life. As expected, infants who were breastfed experienced less diarrhea, lived in wealthier households with better hygiene, and grew faster from B6M. Males with rapid B6M growth reached puberty earlier and, as young adults, had higher testosterone levels, were taller, more muscular, and had higher grip strength. They also had sex earlier and were more likely to report having had sex in the past month, resulting in more lifetime sex partners. Relationships between B6M weight gain and physical outcomes were generally not present or weaker in female subjects. We conclude that rapid weight gain specific to the brief postnatal hypothalamic-pituitarygonadal critical period predicts early maturation and sexual activity, elevated hormone production, and more costly adult somatic characteristics among the male subjects in this sample. These findings provide evidence for early life developmental plasticity in male life history and reproductive strategy in humans.adaptation | developmental plasticity | testosterone | endocrinology | growth and development D evelopmental plasticity in response to nutrients and hormones during fetal and infancy development can modify growth patterns, adult metabolism, and hormone regulation (1, 2). These effects are hypothesized to have evolved to allow modification of nutritional requirements and reproductive strategy as ecological conditions change (3-5). Maternally derived ecological cues transferred via the placenta or in breast milk could convey information about typical energetic or social experiences in the past (5, 6), and thus allow the developing organism to modify biological settings in anticipation of conditions likely to be experienced in the future (3, 4, 7).Although widely cited, this hypothesis has been subjected to minimal empirical testing in humans. A small number of human studies provide evidence for early life plasticity in reproductive biology, which has clear implications for genetic fitness and thus could be under selection. Jasienska and colleagues (8) reported that the threshold of energetic stress that suppresses ovarian steroidogenesis varies according to a woman's own birth weight, and they speculated that this indicates a capacity to reset energetic thresholds regulating initiation of pregn...

Starvation stress during larval development facilitates an adaptive response in adult worker honey bees (Apis mellifera L.)

“…Similar responses to developmental food deprivation have been found throughout the animal kingdom (Lee and Zucker, 1988;Applebaum and Heifetz, 1999;Simpson et al, 1999;Krause et al, 2009;Mitchell et al, 2009;Kuzawa et al, 2010;van den Heuvel et al, 2013). Our study also suggests that mechanisms involved in the responses to larval nutritional stress imposed by nurse bees (young adult workers that feed the larvae) play a key role in honey bee division of labor (Page, 2013).…”

“…In mammals, under-nutrition or over-nutrition during the prenatal or postnatal period can impact adult reproductive capability (reviewed by Gardner et al, 2009), which may reflect an adaptive adjustment of reproductive strategy (Rae et al, 2002;Rhind, 2004;Jasienska et al, 2006;Kuzawa et al, 2010). In general, a strategy of reducing reproductive investment while increasing somatic maintenance is a typical survival mechanism in insects (Elkin and Reid, 2005;García-Roger et al, 2006).…”

“…Studies in several model organisms have suggested that one strategy to overcome such challenges is to have a mechanism that tailors development to produce an adult phenotype adapted to the conditions that the organism encountered during maturation in anticipation of that condition occurring during its adult stage (Krause et al, 2009;Mitchell et al, 2009;Kuzawa et al, 2010;Lee and Zucker, 1988;Simpson et al, 2001;van den Heuvel et al, 2013). For example, desert locust embryos (Schistocerca gregaria) respond to the crowding conditions that their mothers experience (Simpson et al, 2001) by maturing into one of two adult phenotypes that differ in morphology, physiology and behavior (Applebaum and Heifetz, 1999).…”

Nutritional Determinants of the Timing of Puberty

“…In a prospective investigation of 994 Filipino girls, every month of exclusive breastfeeding was associated with a 6% lower probability of menarche over the followup period after adjusting for socioeconomic, maternal, and birth characteristics (3). Contrary to these studies, an investigation of 770 Filipino boys found that those who were breastfed as infants had a faster height velocity from birth to 6 months, which was inversely associated with pubertal maturation, than did boys who were not breastfed (56).…”

Secure Infant-Mother Attachment Buffers the Effect of Early-Life Stress on Age of Menarche

“…Neither fast nor slow strategies are inherently better. Instead, the evolutionary benefit of a given strategy depends on the environment in which an individual develops (Belsky, 1997;Belsky et al, 1991;Caudell & Quinlan, 2012;Kuzawa, McDade, Adair, & Lee, 2010;Simpson & Belsky, 2008, in press). Belsky et al (1991) were the first to specify how lifehistory strategies should unfold across the life span.…”