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The Exposome in Human Evolution: from Dust to Diesel Volume 94, No. 4 December 2019 THE QUARTERLY REVIEW of Biology THE EXPOSOME IN HUMAN EVOLUTION: FROM DUST TO DIESEL Benjamin C. Trumble School of Human Evolution & Social Change and Center for Evolution and Medicine, Arizona State University Tempe, Arizona 85287 USA e-mail: [email protected] Caleb E. Finch Leonard Davis School of Gerontology and Dornsife College, University of Southern California Los Angeles, California 90089-0191 USA e-mail: cefi[email protected] keywords exposome, human evolution, genes, toxins, infections abstract Global exposures to air pollution and cigarette smoke are novel in human evolutionary history and are associated with at least 12 million premature deaths per year. We investigate the history of the human exposome for relationships between novel environmental toxins and genetic changes during human evo- lution in six phases. Phase I: With increased walking on savannas, early human ancestors inhaled crustal dust, fecal aerosols, and spores; carrion scavenging introduced new infectious pathogens. Phase II: Domestic fire exposed early Homo to novel toxins from smoke and cooking. Phases III and IV: Neolithic to preindustrial Homo sapiens incurred infectious pathogens from domestic animals and dense com- munities with limited sanitation. Phase V: Industrialization introduced novel toxins from fossil fuels, industrial chemicals, and tobacco at the same time infectious pathogens were diminishing. Thereby, pathogen-driven causes of mortality were replaced by chronic diseases driven by sterile inflammogens, exog- enous and endogenous. Phase VI: Considers future health during global warming with increased air pol- lution and infections. We hypothesize that adaptation to some ancient toxins persists in genetic variations associated with inflammation and longevity. Correction: This article was corrected and reposted on February 17, 2020, with changes to Table 5. The Quarterly Review of Biology, December 2019, Vol. 94, No. 4 Copyright © 2019 by The University of Chicago Press. All rights reserved. 0033-5770/2019/9404-0001$15.00 333 334 THE QUARTERLY REVIEW OF BIOLOGY Volume 94 Introduction miologic approaches that characterized indi- vidual factors, “one by one” and has become S human ancestors diverged from great widely adapted to approach interactions of A apes, they encountered additional envi- multiple exogenous and endogenous toxins ronmental hazards: increased savanna min- across the lifetime (National Academies of eral dust and fecal aerosols; pathogens from Sciences, Engineering, and Medicine 2017). decaying carrion; smoke from domestic fire; Wild (2012) identified three domains: the ex- new pathogens from domesticated animals ogenous macrolevel (rural versus urban; social in the Neolithic; and, in the Industrial Age, stratification); the exogenous individual (diet, airborne toxins from fossil fuels and tobacco. infections); and the endogenous (biomes, fat During these phases, humans also evolved depots, injuries). The exposome includes all larger brains and extended life histories with stages of life history, from prefertilization prolonged maturation and longer life spans, gametes to development and later life. We as discussed below. Genetic adaptations ac- focus on genes of host defense and brain de- quired during these six million years are velopment during the evolution of the long analyzed in terms of the novel toxins from human life span with its uniquely prolonged exogenous and endogenous sources. Table 1 postreproductive phase. and Figure 1 outline sequential phases of the Evolutionary inquiry of the human expo- expanding human exposome, in which new some illuminates unexplored domains of in- environmental hazards are cumulatively added flammatory processes in the evolution of the to those from prior phases. These new expo- lungs and brain that may inform the future sures need not have occurred at the same of human health and longevity during global time in all human populations, and should warming. Inflammatory responses are near not be considered as hard boundaries for ubiquitous in human adaptations to these the phases. exposures. Many inflammatory responses to The exposome concept was introduced airborne toxins from cigarettes and fossil fu- by Wild (2005, 2012) for comprehensive anal- els are shared with the pathophysiology of ysis of environmental and lifestyle factors in chronic diseases associated with modern air cancer. The exposome extends prior epide- pollution. We hypothesize that adaptation to TABLE 1 Phases in the human exposome Exposome phase, species/ Exposome cumulative progression Chemistry life expectancy, age IA. Pre-Homo/25 y 5–2.5 MYA Dust (mineral), pollen; endotoxins from herd Iron and other toxic metals animals; increased carrion pathogens IB. Early Homo/30 y 2.5–1 MYA II. Early Homo/30 y 1–0.3 MYA Dust, pollen, endotoxins, carrion pathogens; Toxic metals; plus PAH plus domestic biomass smoke and charred meat III. H. sapiens/35–45 y Paleo- to pre- Dust, feces, endotoxins, smoke, charred meat; Toxic metals, PAH; plus endotoxins, infections Neolithic 0.3 MYA-10,000 BP plus human feces IV. H. sapiens/35–45 y Neolithic Dust, smoke, charred meat, human feces; Toxic metals, PAH; plus new endotoxins, 10,000–200 YA plus high-density populations, domestic animal antigens feces, new infections – V. H sapiens/50 85 y Industrial Dust, smoke, charred meat, human and Toxic metals, NH4, PAH, endotoxins, – 1820 2020 animal feces, infections; plus fossil fuels, infections; plus adiposity, CO, O3, NOx, SOx industrial toxins, sugar, tobacco – VI. Future 21st 22nd centuries H. Dust, smoke, charred meat, feces, infections, Transition metals, PAH, NH4, endotoxins, – sapiens/35 90 y global warming fossil fuels, industrial toxins; plus higher O3, infections, O3, NOx, SOx; plus increased and coastal inundation crustal dust, insect-borne infections, migrations, O3, glycoxidation, PAH, temperature water shortages New factors in each phase are italicized. December 2019 THE EXPOSOME IN HUMAN EVOLUTION 335 ancient airborne toxins may be recognized in diverse environments near the southern in modern genetic variations, including the edge of the Sahara, showed early evidence genotypes of cigarette survivors who may of bipedalism (Brunet et al. 2002). Later hom- have genetic resistance to cigarette aerosols. inins, including Ardipithicus ramidus (ap- Inflammation has become an environmen- proximately 4.4 MYA), inhabited a primarily tal byword because inflammatory responses forest and wooded grassland paleoecology are broadly stimulated by molecular damage. (White et al. 2009). We discriminate two broad classes of inflam- Major aridification in East Africa during matory stimulae: pathogen-driven inflammation the last three million years has particular rel- from infectious viruses, microbes, and para- evance to the emergence of Homo (Finch sites versus sterile inflammation from noninfec- 2012). Early habitats gradually shifted from tious toxins and stressors such as cigarette closed canopy forest to open grass- and shrub- smoke or fat depots (Crimmins and Finch land savannas (Feakins et al. 2005; Bonnefille 2006; Finch and Kulminski 2019; Phase V). 2010; Cerling et al. 2011). Savanna grasses Some inflammatory responses are shared generally rely on wind pollination, and thus by infectious pathogenic and sterile inflam- produced more pollen than tropical trees that mogens, as in the toll-like receptor (TLR4) rely on insect or animal pollination (Dupont pathway responses to bacterial lipopolysac- and Wyputta 2003). Thus, novel sources of charides (LPSs) and urban air pollution par- pollen exposure may have increased as grass- ticles (Woodward et al. 2017). The many lands expanded. Arid areas are also major TLR pathways are critical to innate immune sources of dust (Prospero et al. 2002). The ari- responses (“911 standby”), but also to the dification the East African hominin sites is am- slower adaptive immune responses target- ply documented by an increase in windblown ing specific antigens. Innate immune genes dust reaching marine sediments (deMenocal are prominent among the evolved genetic ac- 1995) and by the carbon isotope ratios in pa- commodations in the context of adaptive re- leosols that distinguish woodlands and grass- sistance to pathogens and survival of injury. lands (Sikes 1994; Cerling et al. 2011; Rowan Furthermore, neurodevelopmental processes and Reed 2015; Lüdecke et al. 2018). These employ innate immune mechanisms during changes in foliage were complex and region- brain maturation. Building from these estab- ally diverse, involving Southern Africa and lished findings, we suggest how evolved im- the upper Rift Valley (Levin et al. 2011). Most mune genes may have interacted with new hominid sites were within extensive wood- brain genes. lands (approximately 40%; Reed 1997; Cerling et al. 2011; Rowan and Reed 2015). Poor pres- Exposome Phase I: Savanna Aerosols ervation of bones in forests limits knowledge expanding exposure to dust, pollen, of our early ancestors and their environmen- endotoxins, and carrion pathogens tal conditions. After 3 MYA in the Rift Valley, hominins The African environment has undergone were exposed to seasonal surges in airborne major changes in the last 10 million years dust and pollen (Wood and Lonergan 2008; throughout its vast area (Cerling et al. 2011). White et al. 2009). Fossil evidence suggests The shrinking of the Tethys Sea 7–11 MYA expanding populations of bovines and ro- caused major shifts in the African summer dents 2.7–1.7 MYA with evidence of arid-ad- monsoon (Larrasoaña
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