Contemporary small-scale subsistence populations offer unique insights into human musculoskeletal health and aging

Abstract

Human foragers avoid noncommunicable diseases that are leading causes of mortality, partly because physically active lifestyles promote healthy aging. High activity levels also promote tissue damage accumulation from wear-and-tear, increase risk of injury and disability which compromise productivity, and reduce energetic investments in somatic maintenance given constrained energy expenditure. Constraints intensify when nutrient supply is limited and surplus energy is directed toward pathogen defense and reproduction, as occurred throughout hominin evolution. This paper reviews evidence linking exposomes to musculoskeletal health in subsistence populations, focusing on effects of physical activity, pathogens, diet, and reproduction. Chronic musculoskeletal conditions are common for humans and possibly prehistoric hominins but rarer in quadrupedal apes. We propose that transition to bipedalism ~6 to 8 million years ago constituted an early "mismatch scenario," increasing hominin susceptibility to musculoskeletal conditions vis-à-vis quadrupedal apes due to changes in mechanical loading environments. Mismatched musculoskeletal traits were not targets of selection because of trade-offs favoring bipedal extractive foraging and higher fertility.

Fig. 1.. Opportunities for and risks of accidental self-laceration among Tsimane by age and sex.

Opportunities for laceration are estimated using time allocation data. Stacked bars show proportion of time at risk of self-laceration (n = 55,035 observations of 904 individuals across six villages) from either food processing (e.g., butchering), other household tasks (e.g., sharpening knives or clearing trails with machetes), labor (e.g., building a house or boat, tree chopping, or clearing brush in fields), tool manufacture including children’s play with machetes, and resource acquisition (e.g., harvesting with knives or machetes and hook-and-line fishing). Activities for which there was uncertainty over whether one faced self-laceration risk were omitted from the risk set. Risks of laceration are estimated using a hazard function based on retrospective self-reports among a different Tsimane sample collected contemporaneously as the time allocation data (n = 388 individuals aged 11 to 75 years across 16 villages). The hazard function is modeled separately for each sex using the bshazard package in R, stratifying by episode number to account for repeated lacerations within individuals over time. The blue line shows the mean hazard for each 5-year age interval. F, female; M, male.

Fig. 2.. Current musculoskeletal pain prevalence (age-standardized using the direct method) by sex and population.

The 95% confidence intervals are exact binomial. Populations are shown in descending order of male prevalence. Estimates are derived using an identical minimum age of 15 years across populations. Reproduced from (8). R, rural sample; U, urban.

Fig. 3.. Human female calcium economy (i.e., intake, absorption, and demand; in grams) during a single synthetic reproductive bout composed of gestation and lactation.

(A and C) Minimum and maximum observed calcium intakes, respectively (122). (B) Tsimane intake (123). Calcium absorption is 50% of intake during pregnancy (preg) and 25% during lactation [lact; (142)]. Demand consists of fetal skeletal calcium accretion (30 g at parturition for a full-term 3.5-kg neonate) and daily maternal-infant calcium transfers during lactation. Three periods of lactation are shown: early (first 180 days), middle (mid; subsequent 180 days), and late (final 210 days), signifying the decline in daily maternal-infant transfers over time. Estimated calcium transfers during early and middle lactation periods (i.e., 200 and 120 mg/day, respectively) are from (142). Late period transfers (81 mg/day) are estimated from two recent meta-regressions: (i) breast milk calcium concentration on days since parturition (145) multiplied by (ii) age-specific breast milk intake [see Table 3 in (189)]. Inclusion of the late lactation period reflects prolonged breastfeeding typical of natural fertility populations, using as a benchmark the mean Tsimane weaning time of 19 months (190). Pregnancy is assumed to last 280 days. Maternal calcium intake is assumed to be constant during pregnancy and lactation [cf. (191)]. Calcium absorption efficiency is assumed to be independent of intake and other factors. Maternal calcium demand for maintaining homeostasis is not considered here, and thus, demand is a lower bound estimate.

Fig. 4.. Cumulative net calcium balance (i.e., absorption − demand; in grams) by reproductive status and parity (range: 1 to 10) across variable calcium intakes and periods of maternal recovery following each reproductive bout.

Calcium balance is calculated from the running total across reproductive statuses and bouts. (A and C) Minimum and maximum observed human calcium intakes, respectively. (B) Tsimane intake. Reproductive status includes pregnancy, three periods of lactation, and a NPNL phase. The NPNL phase is the duration from weaning until the next conception and is characterized by zero calcium demand from reproduction. Three NPNL phase durations are shown: 0 months (i.e., no maternal calcium recovery from weaning until the next conception) and 6 and 12 months (see text for additional details). Maternal calcium demand for maintaining homeostasis is not considered here, and thus, demand is a lower bound estimate.