Original Research Article Helminths and Human Ancestral Immune Ecology: What Is the Evidence for High Helminth Loads Among Foragers? DOUGLAS LONDON, 1 * AND DANIEL HRUSCHKA 2 1 Departmentof Anthropology, Adelphi University, Garden City, New York, 11530 2 School of Human Evolution and Social Change, Arizona State University, Tempe, Arizona 85287 ABSTRACT: Objectives: Recent theories of human immune ecology have invoked high helminth loads as an impor- tant selection factor among early humans. However, few studies have assessed this assumption among extant human foragers. Methods: We review the current evidence for high helminth loads in documented forager populations and present new data from members of a Kawymeno Waorani forager group in Amazonian Ecuador (n 5 16) compared with neigh- boring Kichwa subsistence farmers (n 5 63). Results: Stool samples indicated a near absence of helminths among the Kawymeno foraging group (6.25% with Ascaris lumbricoides and 0% with Ancylostoma duodenale or Trichuris trichiura). In contrast neighboring, isolated Kichwa subsistence farmers in a similar ecosystem had abundant helminth infestations (76.1% with Ascaris lumbri- coides, 11.1% with Ancylostoma duodenale, and 1.5% with Trichuris trichiura). The presence of helminths among the Waorani and Kichwa was triangulated across multiple data sources, including presence in stool samples, medical exams, and 3 years of participant observation. Conclusions: These findings, coupled with the modern forager literature, raise questions as to whether helminths were prevalent enough in Paleolithic humans to be a unique evolutionary selective force in human physiology. Am. J. Hum. Biol. 26:124–129, 2014. V C 2014 Wiley Periodicals, Inc. The Helminth Hypothesis proposes that the coexistence of parasitic helminths (multicellular wormlike parasites) in human bodies throughout much of human evolution resulted in the selection of an immune system adapted to helminths that involves the recruitment of a specific anti- body, immunoglobulin E (IgE) (Dunne and Cook, 2005; Fumagalli et al., 2009; Hurtado et al., 2008). According to the hypothesis, recent public health measures to reduce helminth infections have dramatically altered our immune ecology, and consequently, modern human IgE antibody levels have fallen to a fraction of the normal range found throughout most of human evolution. In turn, it follows that the modern absence of helminth- based IgE stimulation has resulted in vulnerability to infectious diseases, allergy, and autoimmune disorders that were once protected against by the presence of a par- asitic helminth–human host relationship in foraging humans (Allen and Maizels, 2011; Rook, 2009; Yazdan- bakhsh et al., 2002). A crucial assumption of the helminth hypothesis is that IgE-stimulating helminths were endemic in early human foraging populations. Helminths belong to a heterogene- ous category of organisms, and different species can pro- voke different human antibody immune responses—some with minimal IgE response and most with multiple types of antibody responses. Helminth species that principally stimulate IgE and also have a common and widespread geographical presence provide some of the more credible evidence to support the helminth hypothesis. These hypo- thetical candidates include Ascaris lumbricoides, Ancylos- toma duodenale, Necator americanus, and Trichuris trichiura helminths. However, laboratory tests routinely demonstrate that many widespread and common hel- minths are not good candidates to support the helminth hypothesis, such as Taenia species (tapeworms) and Enterobius vermicularis (pinworm or threadworm) as these helminths cause less stimulation of IgE, interacting instead with the IgG and IgM antibodies (Hoberg et al., 2000; Warren and Mahmoud, 1975). Most direct comparisons of helminth infestation among foragers and agriculturalists have used archeological data and indicate that helminths may have been rarer in for- ager populations than agricultural populations (Armela- gos and Harper, 2005; Leles et al., 2010; Reinhard, 1988; Reinhard and Araujo, 2012; Reinhard et al., 1985). Most archeological evidence supporting human–helminth coex- istence postdates the development of extensive agricul- ture (Sianto, 2009) and indicates that domestication of plants and animals in Neolithic farming cultures likely facilitated the spread of parasites that may have existed only sporadically in foragers (Cockburn, 1971; Kunitz, 1983; McKeown, 1976; Sianto, 2009). Interestingly, the most concrete evidence of Paleolithic helminth–human coexistence is found for two types of helminths—Taenia species (tapeworms) and Enterobius vermicularis (pin- worm or threadworm) (Ferreira et al., 1997; Hoberg et al., 2000, 2001; Hugot et al., 1999; Shipman, 2002), both of which only minimally stimulate IgE. Although there have been Ascaris lumbricoides and Ancylostoma duodenale helminths found in South American mummies (Allison Contract grant sponsor: Wenner-Gren Foundation; Contract grant num- ber: 8055; Contract grant sponsor: Fulbright Foundation; Contract grant number: 34117326. *Correspondence to: Douglas London, Department of Anthropology, Adelphi University, 1 South Street, Blodgett Hall 102, Garden City, NY 11530, USA. E-mail: dlondon@adelphi.edu Received 6 September 2013; Revision received 20 December 2013; Accepted 22 December 2013 DOI: 10.1002/ajhb.22503 Published online 28 January 2014 in Wiley Online Library (wileyonlinelibrary.com). V C 2014 Wiley Periodicals, Inc. AMERICAN JOURNAL OF HUMAN BIOLOGY 26:124–129 (2014)