medRxiv preprint doi: https://doi.org/10.1101/2020.09.10.20191916; this version posted September 11, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license . 1 Productivity loss associated with physical impairment in a contemporary small-scale 2 subsistence population 3 4 5 Jonathan Stieglitza,b*, Paul L. Hooperc, Benjamin C. Trumbled,e, Hillard Kaplanc, Michael D. 6 Gurvenf 7 8 9 *Corresponding author, at the following postal address: 10 Institute for Advanced Study in Toulouse 11 1 esplanade de l'Université 12 T.470 13 31080 Toulouse Cedex 06, France 14 Phone: +33 6 24 54 30 57 15 E-mail: [email protected] 16 17 18 19 Author affiliations: 20 aUniversité Toulouse 1 Capitole, 1 esplanade de l'Université, 31080 Toulouse Cedex 06, France 21 bInstitute for Advanced Study in Toulouse, 1 esplanade de l'Université, 31080 Toulouse Cedex 22 06, France 23 cEconomic Science Institute, Chapman University, 1 University Drive, Orange, CA, 92866, USA 24 dCenter for Evolution and Medicine, Life Sciences C, 427 East Tyler Mall, Arizona State 25 University, Tempe, AZ, 85281, USA 26 eSchool of Human Evolution and Social Change, 900 South Cady Mall, Arizona State 27 University, Tempe, AZ, 85281, USA 28 fDepartment of Anthropology, University of California, Santa Barbara, CA, 93106, USA 29 30 31 32 Acknowledgements 33 We thank the Tsimane for participating and THLHP personnel for collecting and coding data. 34 We also thank the HORUS Study Team for assistance with CT data collection. Amélie Beaudet, 35 Susan Pfeiffer, George Perry and an anonymous reviewer provided useful comments that 36 improved the quality of the manuscript. Bone strength estimates used in this study were 37 generated under the supervision of Matthew Budoff. Funding was provided by the National 38 Institutes of Health/National Institute on Aging (R01AG024119), National Science Foundation 39 (1748282), the Center for Evolutionary Medicine at Arizona State University, and the University 40 of California-Santa Barbara Academic Senate. JS acknowledges IAST funding from the French 41 National Research Agency (ANR) under the Investments for the Future (Investissements 42 d’Avenir) program, grant ANR-17-EURE-0010. Funding sources had no role in research 43 conduct, study design or article preparation. 44 45 1 NOTE: This preprint reports new research that has not been certified by peer review and should not be used to guide clinical practice. medRxiv preprint doi: https://doi.org/10.1101/2020.09.10.20191916; this version posted September 11, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license . 46 Abstract 47 Humans experience unique physical impairments with potentially severe economic 48 consequences. Quantifying the burden of impairment in subsistence populations is critical for 49 understanding selection pressures underlying strategies that minimize risk of production deficits. 50 We examine among forager-horticulturalists whether compromised bone strength (indicated by 51 vertebral fracture and lower bone mineral density, BMD) is associated with diminished 52 subsistence involvement. We estimate the magnitude of productivity losses associated with 53 compromised bone strength. Fracture is associated with cessation of hunting, tree chopping and 54 walking long distances, but not tool manufacture. Age-specific productivity losses from hunting 55 cessation related to fracture and lower BMD are substantial: ~397 lost kcals/day, with expected 56 future losses of up to 1.88 million kcals (22% of expected production). Productivity loss is thus 57 substantial for high strength and endurance tasks. Determining the extent to which impairment 58 obstructs productivity in contemporary subsistence populations improves the ability to infer 59 consequences of impairment over human evolution. 60 61 Keywords: Physical impairment, skeletal gracility, life history theory, vertebral fracture, bone 62 mineral density, Tsimane 63 64 65 66 67 68 2 medRxiv preprint doi: https://doi.org/10.1101/2020.09.10.20191916; this version posted September 11, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license . 69 1. Introduction 70 As the longest living and slowest growing primate, humans experience unique physical 71 impairments with potentially severe economic and social consequences. Human hunter-gatherers 72 have lower adult mortality than chimpanzees and a significant post-reproductive lifespan 73 (Gurven and Kaplan 2007; Hill et al. 2007; Kaplan et al. 2010; Kaplan et al. 2000; Wood et al. 74 2017), which generates ample opportunity for incident degenerative disease and dysfunction 75 (Finch 2010). Evidence at least 2 mya of greater dietary reliance by hominins on difficult-to- 76 acquire resources including hunted game (Aiello and Wheeler 1995; Antón et al. 2014; 77 Thompson et al. 2019; Ungar 2012) suggests delayed peak skill acquisition in adulthood (Gurven 78 et al. 2006; Kaplan et al. 2000; Koster et al. 2019; Walker et al. 2002), possibly when physical 79 senescence is already underway. Adult physical impairment (hereafter API) of degenerative 80 origin thus has the potential to hinder hominin foraging in costly ways. These costs amplify if 81 API hinders resource transfers or provisioning of other assistance, given their potential fitness 82 impacts (Gurven et al. 2012; Hawkes 2003; Hill and Hurtado 2009; Hooper et al. 2015; Marlowe 83 2003; Schniter et al. 2018; Wood and Marlowe 2013). The ubiquity among hunter-gatherers to 84 form social groups of clusters of multi-generational resource-pooling units (Kaplan et al. 2009; 85 Migliano et al. 2017), and in base camps at least ~400 kya (Kuhn and Stiner 2019), may reflect a 86 species-typical strategy of complex cooperation to minimize daily risks, including production 87 shortfalls. Quantifying the burden of API in terms of productivity loss in extant small-scale 88 subsistence populations is thus critical for understanding the strength of selection pressures for 89 cooperative strategies that minimize risks associated with disability. 90 Skeletal evidence indicates that API of degenerative origin was not uncommon 91 throughout hominin evolution, and that API likely interfered with activities essential for survival 3 medRxiv preprint doi: https://doi.org/10.1101/2020.09.10.20191916; this version posted September 11, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license . 92 and reproduction (e.g. bipedal locomotion, food acquisition, load carrying). For example, marked 93 thoracic kyphosis and vertebral disc degeneration are evident in Australopithecus afarensis (AL- 94 288) from ~3.2 mya (Cook et al. 1983), as is spondylolisthesis in middle Pleistocene humans 95 (SH-1) from ~430 kya ((Bonmatí et al. 2010); also see (Trinkaus 2018)). These ailments 96 regularly cause lower back pain, difficulty walking, and carrying or lifting objects among 97 modern clinical patients, who may provide indirect insight into API-related consequences in past 98 hominin populations. Given the variability across hominin species in terms of environmental 99 exposures, diet, life history traits (e.g. lifespan), morphology (e.g. body and brain size) and 100 locomotion from ~4 mya until 40 kya (Wood and K. Boyle 2016), whether and how these 101 ailments hindered survival and reproduction is unclear, and not readily discernable from any 102 single hominin species. 103 Joint behavioral and epidemiological study of contemporary small-scale subsistence 104 populations suggests that diverse ailments of degenerative or other etiology hinder resource 105 production and transfers. Among Yora forager-horticulturalists of Peru, men are unable to forage 106 due to illness or injury on 11% of all days (Sugiyama and Chacon 2000). Among Shiwiar 107 forager-horticulturalists of Ecuador, ~90% of individuals experience an ailment (e.g. chronic 108 pain, fracture, laceration, infection, animal bite or sting, burn) severe enough to interfere with 109 subsistence work for ≥2 weeks, and >60% experience API for ≥1 month; suspected bone 110 fractures – a focus of the current study – are more likely than other ailments to cause prolonged 111 disability (Sugiyama 2004). Among Tsimane forager-horticulturalists of Bolivia, the population 112 studied here, 75% of adults report being bedridden due to illness or injury at least once in the 113 three months prior to survey, and Tsimane are incapacitated on about 10% of all days (Gurven et 4 medRxiv preprint doi: https://doi.org/10.1101/2020.09.10.20191916; this version posted September 11, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license . 114 al. 2012). The fact that these studies