Evolutionary Anthropology 23:218–228 (2014)

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Parasites and Human Evolution GEORGE H. PERRY

Our understanding of human evolutionary and population history can be advanced by ecological and evolutionary studies of our parasites. Many parasites flourish only in the presence of very specific human behaviors and in specific habitats, are wholly dependent on us, and have evolved with us for thousands or millions of years. Therefore, by asking when and how we first acquired those parasites, under which environmental and cultural conditions we are the most susceptible, and how the parasites have evolved and adapted to us and we in response to them, we can gain considerable insight into our own evolutionary history.1,2 As examples, the tapeworm life cycle is dependent on our consumption of meat,3 the divergence of body and head lice may have been subsequent to the development of clothing,4,5 and malaria hyperendemicity may be associated with agriculture.6 Thus, the evolutionary and population histories of these parasites are likely intertwined with critical aspects of human biology and culture. Here I review the mechanics of these and multiple other parasite proxies for human evolutionary history and discuss how they currently complement our fossil, archeological, molecular, linguistic, historical, and ethnographic records. I also highlight potential future applications of this promising model for the field of evolutionary anthropology.

The parasite proxy approach aims to make indirect inferences about the evolutionary history of a host species (in our case, humans) through the study of organisms with which the host species is commonly and intimately associated.7 One strict definition of “parasite” is an organism that lives on or in another spe-

George (PJ) Perry is an Assistant Professor in the Departments of Anthropology and Biology and a faculty member of the Ecology and Bioinformatics & Genomics interdisciplinary graduate programs at Pennsylvania State University. His group’s research is broadly concerned with human and nonhuman primate evolutionary ecology and genomics. E-mail: [email protected]

Key words: hominin evolution; human population history; agricultural transition; tapeworms; lice; hookworms; malaria

C 2015 Wiley Periodicals, Inc. V

DOI: 10.1002/evan.21427 Published online in Wiley Online Library (wileyonlinelibrary.com).

cies, feeds on that species, causes it some harm, and has adapted to it in some fashion.8 In this paper, I use a more inclusive definition of parasite that encompasses bacteria and viruses, which are sometimes separately classified, as well as behavioral parasites9 (or “commensals”) such as rats, out of recognition that these organisms can also be intimately associated with humans and that, in consequence, their histories can also inform us about our own. I typically discern three principal types of parasite proxy analysis, each offering different but potentially complementary forms of insight into human evolution: 1) determining when and from which other host species we acquired our parasites, 2) inferring parasite population and demographic histories, and 3) studying how parasites have adapted to the human biological and ecological environment. This review provides a brief overview of each type of analysis, followed by a discussion of spe-

cific published and potential future parasite proxy studies of human evolution, structured by time period. 1) Host species transfers are relatively rare for many parasites,10–12 such that these events can often be distinguished from more typical patterns of host-parasite phylogenetic concordance, although there are other generalist parasites that may repeatedly infect multiple different host taxa.13–15 We know that host transfers and generalist sharing both occur more commonly, although not exclusively, among phylogenetically similar host species.12,16,17 Regardless, when parasite transfers between host species do occur, this implies spatiotemporal contact between the host species involved. Susceptibility to specific parasites may also require a certain host environment and behavior, facilitating inferences about host evolutionary ecology. Thus, many anthropological applications of the parasite proxy approach have centered on the estimation of parasite phylogenies and species divergence times for subsequent consideration in the context of potentially associated events in hominin evolutionary history (Fig. 1). Direct archeological, and especially fossil evidence, of parasites is rare. Consequently, divergence date estimates typically are based on the application of a molecular clock to the proportion of nucleotide differences between two or more parasite DNA sequences. Unfortunately, in the absence of fossil data, parasite molecular clock calibrations and mutation rate inferences are not straightforward, as perhaps is best illustrated by the history of analyses of the malaria parasites Plasmodium falciparum and P. vivax (Box 1). This

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Figure 1. Parasite host species transfers inform hominin evolutionary history. The timing of selected parasite host species transfers and their potential proxy significance (in parentheses), superimposed on an approximate hominin phylogeny. Original hosts are shown at right. The original host for human Plasmodium vivax may have been either gorilla or chimpanzee106; for simplicity, only gorilla is shown. All fossil, parasite, and original host depictions were modified from images on Wikimedia Commons. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

inherent challenge must be kept in mind when interpreting parasite divergence date estimates. 2) Once a parasite has been transferred to humans, its intraspecific history may track and inform our own population dynamics. For exam-

ple, if parasites were inadvertently transported to newly colonized lands by their hosts, then parasite population splits may reflect human migration events. Similarly, we may observe signatures of contact between previously isolated human

populations in the form of modern parasite biogeographic patterns. In fact, analyses of parasite population history could, in some cases, be more sensitive than modern human population genetics for detecting potential contact among human

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Box 1. Human Malaria Parasite Molecular Clock Challenges The history of phylogenetic misassumptions and molecular clock challenges for human Plasomidum malaria parasites illustrates the importance of comprehensive sampling and, in the absence of a parasite fossil record, the cautious interpretation of parasite proxy data. Specifically, Plasmodium falciparum was long thought to be most closely related to P. reichenowi, a malaria parasite of chimpanzees (Pan troglodytes), with commensurate parasite and host divergence.99 P. falciparum demographic events were therefore dated under a Plasmodium molecular clock calibrated, in part, with a hominin fossil-record-supported date of 6 MYA for divergence between the P. falciparum and P. reichenowi lineages.100 However, from a series of recent publications that extensively sampled African apes (reviewed in Prugnolle and coworkers101), we now instead have some confidence that i) human P. falciparum is, in fact, very closely related to a clade of gorilla malaria parasites and ii) that there is substantially greater genetic diversity in the gorilla Plasmodium clade than among human P. falciparum sequences.102 Together, these findings suggest a relatively recent host transfer from gorillas to humans. A transfer within the time frame of the agricultural transition would be consistent with the notion that associated environmental modifica-

populations, since parasite transmission could theoretically occur even in the absence of any human gene flow. Other relevant parasite population phenomena, including expansions and bottlenecks, may follow human demographic history. 3) Parasites live on, inside, or in association with their host species. Therefore, they must be able to survive in a host-specific ecological and biological context. After an initial

tions (such as irrigation) and increased human population densities would have exacerbated susceptibility to falciparum malaria.6 The timing of natural selection for human mutations that provide resistance to P. falciparum infection is also consistent with the origins of agriculture.103 However, human falciparum malaria could still have predated agriculture, but without the strong selection pressures associated with subsequent agricultureassociated malarial hyperendemicity. Unfortunately, given the newly revised phylogeny, the prior molecular clock calibrations and resulting date estimates were off by unknown factors, so we are currently unable to date the gorilla-tohuman Plasmodium falciparum host species transfer and evaluate the concordance of this date with the origins of agriculture in Africa. The recent discovery of a lemur Plasmodium species104 could ultimately facilitate the calibration of a more accurate molecular clock, if one assumes that this parasite diverged from related primate malarias when lemurs initially colonized Madagascar. Given the history of molecular clock challenges, I am unready to make this assumption. There is a similar history of revision concerning the evolutionary origins of the other major human malaria parasite, Plasmodium vivax. With limited comparative

host species transfer, a parasite might have adapted to its new environment, then continued to adapt in response to host biological or ecological changes (Box 2). The coevolutionary association between parasite and host presents an amazing, largely untapped opportunity to make indirect inferences concerning human evolutionary biology and behavioral ecology through the study of human-specific parasite adapta-

sampling, P. vivax was inferred to have originated in Asia via a macaque-to-human host species transfer.105 However, with recent, extended sampling, malaria lineages similar to P. vivax were found in both gorillas and chimpanzees, but with much more diversity in the great ape lineages.106 This result suggests an African origin for vivax malaria, followed by a gorilla- or chimpanzee-to- human host species transfer.106 While agriculture may have exacerbated vivax malaria endemicity, several lines of evidence indicate that this host species transfer likely predated the agricultural transition. Human vivax malaria is now precluded from sub-Saharan Africa due to near-fixation of the protective Duffy-null allele.107 Patterns of genetic diversity around the Duffy locus suggest an older origin for the Duffy-null mutation.108 If the fixation reflects a history of positive selection due to vivax malaria resistance, then that history likely began before agriculture.109 Human P. vivax is approximately twice as genetically diverse as P. falciparum, which is consistent with a more ancient host species transfer.110 The recurring nature of vivax malaria, as well as its longer incubation period and lower virulence than falciparum malaria,111 may have more readily facilitated stable infections in human huntergatherer populations.109

tions. This form of parasite proxy analysis has strong potential for future evolutionary anthropology research.

HOMININ EVOLUTION Longstanding human parasites can offer insights into the deeper periods of our evolutionary history, thereby complementing the hominin fossil record. The fossil record itself is, of course, incomplete, precluding a

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definitive understanding of our phylogenetic and skeletal evolutionary history. It is even more difficult, from the fossil record alone, to draw inferences about nonskeletal biology, evolutionary ecology, and behavior. Finally, while human genome and archaic hominin ancient DNA analyses can be helpful in some of these respects, for genetic changes that are not variable within living species (that is, genetic differences that are fixed between humans and chimpanzees), it is intrinsically difficult to equate genotype to phenotype or, for mutations with known phenotypic relevance, to infer when those mutations occurred. Therefore, parasite proxy analyses that can advance our knowledge of these challenging to understand, early periods of hominin evolution are particularly valuable to evolutionary anthropologists.

Tapeworms and Hominin Dietary Evolution The earliest purported evidence of hominin meat-eating behavior in the fossil record is from Dikika, Ethiopia, at 3.39 MYA. The evidence, consisting of cut and percussion marks on an ungulate rib and a bovid femur,18 has been questioned.19 There are also undisputed humaninduced cut and percussion marks on the medial surface of a bovid mandible and femur at 2.5 MYA from near Gona, Ethiopia.20 Are these rare examples of hominin carnivory or do they indicate that a major, consistent dietary shift had occurred by 2.5-3.4 MYA? Did the origins of large-scale hominin meateating behavior occur even earlier in our evolutionary history? Since the maintenance of distinct tapeworm lineages requires consistent consumption (that is, in every generation) of animal tissue, studies of human-specific tapeworm parasites have the potential to contribute to our understanding of this issue. Tapeworms have a complex life cycle that requires both definitive (carnivore) and intermediate (typically herbivore) hosts. The adult worm is attached to the intestine of the definitive host and releases eggs or eggcontaining proglottids into feces.

Following herbivore (intermediate host) egg ingestion, larval cysts develop in muscle or other tissues and are then consumed by the carnivore, resulting in new infection. Three tapeworm species primarily parasitize humans: Taenia asiatica (intermediate host, pigs) and T. saginata (cattle) are closely related sister species, while T. solium (pigs) is morphologically distinct.21 The traditional thought was that humans acquired these tapeworm species sometime within the last 12 ky, commensurate with pig and cattle domestication.22,23 In this scenario, pigs and cattle were the long-term intermediate hosts, with nonhuman carnivores the definitive hosts before a recent definitive host species shift to humans. However, a more recent morphological analysis of 35 tapeworm species suggested that the species most

human-specific tapeworms may have evolved to withstand the high heat stresses associated with cooking meat

closely related to T. solium was a hyena tapeworm (T. hyaenae) and that the species most closely related to T. asiatica and T. saginata was a lion tapeworm (T. simbae), both with bovid intermediate hosts.3 Thus, our hominin ancestors may have originally acquired tapeworms through more ancient definitive host shifts while they were hunting or scavenging on the same bovid species as hyenas and lions. In this scenario, there was a much more recent intermediate host shift to pigs and cattle, mediated by humans, following their domestication. If this hypothesis is correct, then divergence of the three human tapeworm species from the lion and hyena tapeworms must have occurred either commensurate with or subsequent to the onset of consistent, large-scale hominin meat-eating behavior. We

still lack a full conclusion to this story. Using a tapeworm-specific molecular clock, Knapp and colleagues24 estimated a 0.6 MYA divergence of the human T. asiatica and T. saginata tapeworms, so the divergence of T. simbae from this clade must have been earlier. Unfortunately, however, nucleotide sequence data from T. hyaenae and T. simbae are not yet available. These data would facilitate the most informative analyses with respect to hominin evolution. Another opportunity with tapeworms concerns the history of hominin food-cooking behavior. I hypothesize that the human-specific tapeworms may have evolved to withstand the high heat stresses associated with cooking meat. Experimental data have shown that Taenia saginata cysts heated to 50 C for 5 minutes are unaffected, whereas those heated to 53–54 C experience some loss of viability and all cysts heated to 56 C are killed.25 Comparative data for nonhuman Taenia cysts are not yet available, but it is straightforward to envision a major selective advantage for a human tapeworm with mutations allowing it to survive inside more fully cooked muscle tissue compared to a tapeworm without such mutations. Recently, Tsai and coworkers26 published the nuclear genome sequences of four tapeworms, including T. solium (the only Taenia species in their study). Among other observations, they described an expansion of the heat shock protein 70 (Hsp70) gene family in T. solium, with 32 intact copies, compared to a maximum of 22 copies among the other genomes. For a tentative functional explanation, we can turn to the intertidal oyster Crassostrea gigas, the genome of which contains 88 intact Hsp70 genes.27 Under experimental heat conditions (35 C), oyster Hsp70 gene expression increases up to 2,000-fold; these gene duplications may aid the organism’s survival during intense sun exposure at low tide.27 Although we lack experimental and sufficient comparative genomic data for human tapeworms, the expanded Hsp70 repertoire in T. solium could confer a similar benefit, but to help protect against cooking-

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Box 2. Host Biological and Cultural Adaptations to Parasite Infection: Parasite Proxy Implications Following host species transfer, parasites may adapt in response to host biological or cultural changes that are unrelated to the parasite but still affect its fitness, or eventually, that evolve in response to the parasite. The latter scenario may be part of an “evolutionary arms race” between parasite and host,112 in which parasites, typically with much faster generation times and larger population sizes, often may have the advantage. However, if any host biological or cultural adaptations to the parasite are sufficiently effective, then the parasite could be eradicated from the host population or species. This possibility has implications for parasite proxy analyses; that is, the absence of a type of parasite in a particular host population or species does not necessarily signify that the host’s ecological history did not include the requisite factors necessary for parasite infection.

related heat stress. Thus, confirming the functional roles of the Hsp70 duplications, or of other humanspecific Taenia molecular changes that enhance heat resistance, and genetically dating them could advance our understanding of the origin of hominin cooking behavior, a subject about which there is considerable debate.28–31 Alternatively, or in addition to this evolutionary hypothesis, tapeworm Hsp70 gene repertoires may have evolved in response to the variable external environmental conditions that proglottids must survive between fecal deposition and herbivore ingestion.

Lice, Loss of Body Hair, Archaic Hominin Contact, and Clothing Humans are parasitized by two species and three types of lice: the pubic louse, Pthirus pubis, and head and body lice, Pediculus humanus. Human head and body lice are morphologically and genetically most similar to the chimpanzee louse,

While direct evidence of past parasite eradication as a result of human biological adaptation is understandably lacking, the relationship between the Duffy-null mutation and Plasmodium vivax malaria can be used to illustrate this concept. As discussed in Box 1, it now appears likely that vivax malaria initially infected humans in sub-Saharan Africa, with the current absence of the parasite in the region explained by the high frequency of the protective Duffynull allele. However, before the recent discovery of P. vivax in African apes,106 the geographic pattern of current human infection led some scientists to favor a scenario in which human P. vivax was never present in sub-Saharan Africa.111 Guinea worm (Dracunculus medinensis) infection and changes in water filtration and use behaviors113 provide an example of the eradication or near-eradication of parasites through cultural adaptation.

Pediculus schaeffi.32 The human and chimpanzee Pediculus lice diverged at an estimated 5.6 MYA,32 based on a molecular clock that assumed a 22.5 6 2.5 MYA divergence of Pediculus spp. and the baboon louse Pedicinus hamadryas (i.e., coincident with the hominoid-cercopithecoid split). Thus, the divergence of the human and chimpanzee Pediculus parasites appears to have been concordant with host speciation. In contrast, the human pubic louse shares morphological similarities and a most recent common genetic ancestor with the gorilla louse, Pthirus gorillae.33 Based on mtDNA sequence data, these two parasite species diverged an estimated 3.32 MYA (95% credibility interval: 1.84-5.61 MYA),33 implying a host species transfer in the Pliocene. Since the lice life cycle does not include a free-living phase, the inferred Pthirus host species transfer would imply spatiotemporal overlap and physical contact between hominins and ancestral gorillas, probably

While the guinea form and other known examples are obviously recent, effective cultural adaptations to parasite infection114–117 could have likewise occurred at earlier periods in hominin evolution. In fact, such behaviors are not even limited to humans.118 For example, chimpanzees appear to recognize the symptoms of intestinal worm infection119 and respond by swallowing whole leaves with roughened surfaces, which is an otherwise uncommon practice.120,121 The leaves pass intact through the digestive system and may mechanically detach intestinal worms.120 Auto-grooming and socialgrooming behaviors, which have been observed extensively among nonhuman primates, also likely represent cultural adaptations to ectoparasite infection.122,123 Thus, both biological and cultural mechanisms may have mediated parasite infection process and patterns throughout hominin evolutionary history.

between 4 and 3 MYA. A dearth of fossils makes it impossible to confidently reconstruct Pliocene gorilla habitats, and reconstructions of hominin paleoenvironments have been controversial.34–36 Nevertheless, given the absence of hominin and gorilla fossil co-occurrence at sites in eastern or southern Africa and the tropical forest habitats of modern gorillas, the Pthirus lice speciation pattern suggests that our hominin ancestors may have inhabited a more diverse range of environments than typically is assumed. While we cannot yet be certain of the Pthirus host species transfer direction, the absence of full body hair on humans provides two discrete, natural lice environments versus only one for gorillas. The loss of human body hair but maintenance (or secondary development) of pubic hair may have made possible a gorilla-to-human host species transfer.33,37 If this scenario is correct, we could infer that the loss of thick human body hair and, potentially,

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the associated development of our evapotranspiration thermoregulatory system38,39 occurred relatively early in hominin evolutionary history. Inferences from species-level phylogenetic relationships are not the only lice proxy application for reconstructing hominin evolutionary history. Specifically, the divergence and geographical patterning of Pediculus humanus genetic lineages suggests interaction between anatomically modern humans and archaic hominin populations or species. Specifically, three major, distinct mtDNA lineages of human Pediculus humanus have been identified from worldwide samples of head and body lice.4,32 One lineage (A) has a worldwide distribution; the second (B) is primarily restricted to the Americas; and the third lineage (C) has been sampled only in Nepal and Ethiopia. Interestingly, the divergence estimates for the three lineages are from 1–2 MYA.40 Reed and colleagues32 hypothesized that the distinct lice lineages reflect parapatric archaic hominin population isolation or speciation, with lineage (A) parasitizing the ancestors of modern Homo sapiens and lineage (B) parasitizing an archaic hominin population that left Africa during the mid-Pleistocene. Later, following the modern human expansion Out of Africa, our ancestors may have come into contact with the surviving archaic hominin species or population, facilitating the transfer of lineage (B) lice to H. sapiens. The geographically restricted pattern of lineage (B) suggested to these authors that the contact may have occurred in East Asia before the peopling of the Americas, requiring the subsequent loss of lineage (B) in Asia. Impressively, the publication of this result predated our recently expanded level of appreciation of Late Pleistocene hominin species’ population diversity and spatiotemporal overlap.41–43 The relationship between head and body lice may provide insight into the origins of clothing, which has an uncertain history prior to the archeological appearance of awls, which were likely used for relatively sophisticated clothing production 70 kya.44 Body lice live and lay eggs on cloth-

ing, but then feed on the body. Today, body lice are rare outside of refugee camps, prisons, or other situations without regular clothing changes and washing. Such conditions presumably were more common earlier in our history. Human head and body lice share a relatively recent common ancestor, with the mtDNA lineages of all body lice found within the Pediculus humanus lineage (A).40 The divergence of body lice, and thus a minimum date for the origins of clothing, has been estimated at 107 kya from mtDNA only45 and at 83–170 kya (95% highest probability density: 29– 691 kya) from combined mtDNA and nuclear markers.46 Whether there were multiple independent origins of body lice from head lice5 is an interesting question that should eventually be clarified by nuclear population genomic studies.47

HUMAN POPULATION HISTORY Multiple lines of evidence support a sub-Saharan African origin for anatomically modern humans (Homo sapiens), followed by expansions to other continents and limited but interesting patterns of interbreeding with Eurasian archaic hominin populations or species.43,48,49 The earliest undisputed anatomically modern human skeletal remains have been recognized in Africa 160 kya,50 SE Asia 46 kya,51 Europe 42 kya,52 and the Americas 12–13 kya.53 Population genetic diversity decreases with increasing geographical distance from East Africa in a pattern consistent with a twowave serial founder effect Out of Africa model.54–56 Genetic and paleogenomic data show that the Americas were originally founded by a relatively small number of total migrants from Siberia.53,57 Archeology-calibrated linguistic data suggest that Polynesia, New Zealand, and Madagascar were (at least in part) founded via an Austronesian expansion that originated in Taiwan 5,230 years BP (95% highest probability density: 4,750-5,800 BP).58 Population divergence and demographic studies of multiple parasites have enhanced our understanding of human population history. For example, Helicobacter pylori is a common stomach bacterium with nearly ubiq-

uitous infection rates in many developing countries. Infection typically is passed from mother to child.59 At a broad global scale, relationships among H. pylori strains have a pattern similar to that of human genetic diversity, supporting the Out of Africa model for modern human origins.60 Furthermore, Khoisan huntergatherers of southern Africa have both the greatest H. pylori lineage diversity61 and the greatest human genomic diversity62 of any studied population. Helicobacter pylori reportedly is present in the stomach of a preColombian mummy63 and H. pylori lineages similar to those found in East Asians are observed among indigenous Americans.64 In combination, these observations are consistent with our current understanding of the original peopling of the Americas. While other modern Native American H. pylori sequences are similar to those from Africa, dating estimates confirm that they reflect recent trans-Atlantic slave-trade population movements.64 Polynesian H. pylori sequences represent a subset of the diversity observed among indigenous Taiwanese populations,65 supporting the Taiwan-origin model of the Austronesian expansion. Our understanding of this expansion has been enhanced through genetic studies of Pacific rat (Rattus exulans) and New Guinea skink (Lipinia noctua) behavioral “parasites” (commensals) that were purposefully or accidentally transported on boats to newly colonized islands.66–68 For some questions these models can be more informative with regard to some questions than studies of modern human diversity or the archeological record,69 given the higher levels of ancestral genetic variation for the behavioral parasites and their shorter generation times, which facilitate faster population growth upon new island colonization. For example, skeletal evidence of an expanding rat population may be easier to detect than sparse material culture evidence of the first human generations. Rats are also voracious seed predators, to the point that they are considered the critical factor in alternative hypotheses of ecological change on Rapa Nui island.70 On New Zealand, Wilmshurst and

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colleagues71 dated both subfossil rat bones and rat-gnawed palm tree seeds relative to a control sample of ungnawed and bird-cracked seeds. Their data suggested the widespread presence of rats across the island by 800 BP,71 providing indirect evidence of human colonization by this time. In contrast to the Helicobacter pylori, skink, and rat examples described above, which augment and generally support previous inferences, hookworm spatiotemporal distributions seemingly promote the consideration of an alternative to the traditional Bering Land Bridge model of the population history of the Americas. Two species of hookworms, Ancylostoma duodenale and Necator americanus, parasitize humans. Both are found in sub-Saharan Africa, Asia, Oceania, and the Americas.72 Hookworms have

a single-host life cycle that includes an environmental phase. Adult worms reside in the human small intestine and deposit eggs into feces, which then in the soil develop into larvae. Larval maturation requires at least five days and a minimum soil temperature of 17 C.73 Once mature, larvae can enter a new human host through contact with bare skin. A. duodenale hookworms have been observed in the small intestine of a 1,100 BP mummy from Peru.74 Hookworm eggs that could not be identified to species were identified in multiple pre-Columbian sources, including human coprolites from 7,200 BP in Brazil75 and 2,200 BP in Tennessee,76 as well as in a 6001,200 BP mummy in Brazil.77 These dates are significant because the soil of the Bering land bridge, the likely migration route for the initial peopling

of the Americas, probably was never sufficiently warm to support the environmental phase of the hookworm life cycle.73,78 Are the pre-Columbian hookworm dates and paleoclimate data inconsistent with a Beringian land migration scenario79 for the initial peopling of the American continent? Would eight years, the maximum hookworm life span,73 be sufficient for a Beringia coastal migration model80 of the peopling of the Americas? Alternatively, could there have been hookworm transfer via cross-Pacific contact with East Asian81 or Polynesian82 populations subsequent to the initial peopling of the Americas but before European contact? Before drawing strong conclusions from the archeological hookworm data, further study is required. First, genetic data from purported preColumbian samples would determine

TABLE 1. Potential Links Between Agriculture and Infection Rates for Selected Human Parasites Parasite Ecological factor and hypothesized consequence

Common name

Proximity to livestock – increased transmission of parasites with secondary herbivore hosts

tapeworm

Higher insect densities due to livestock and standing water habitats, plus higher human population densities and permanent settlements – increased transmission of insect vector parasite infections

loiasis river blindness sleeping sickness leishmaniasis Chagas disease malaria lymphatic filariasis

Sedentary human populations exposed to consistent water sources – increased transmission of parasites with water-borne phases

Permanent human settlements – increased transmission of fecesdependent parasites

Grain storage – increased density of rodent behavioral parasites and exposure to rodent vector parasites and pathogens (partial list)

guinea worm schistosomiasis

paragonimiasis clonorchis hookworm roundworm whipworm amoebiasis giardia mouse rat plague salmonellosis rat-bite fever Lassa fever

Species name Taenia solium Taenia saginata Taenia asiatica Loa loa Onchocerca volvulus Trypanosoma brucei Leishmaniasis spp. Trypanosoma cruzi Plasmodium falciparum Plasmodium vivax Wuchereria bancrofti Brugia malayi Brugia timori Dracunculus medinensis Schistosoma haematobium Schistosoma mansoni Schistosoma japonicum Paragonimus westermani Clonorchis sinensis Ancylostoma duodenale Necator americanus Ascaris lumbricoides Trichuris trichiuria Entamoeba histolytica Giardia duodenalis Mus spp. Mastomys natalensis Rattus spp. Yersinia pestis Salmonella spp. Streptobacillus moniliformis Spirillum minus Lassa virus

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whether they are indeed hookworms83 and, if so, whether they are A. duodenale, N. americanus, or a different species that would indicate an independent host species transfer from an endemic New World mammal to Native Americans. The hypothesis that A. duodenale larvae may occasionally be passed through breast milk to children84 should also be considered, since this could have prolonged the cross-Beringian survival of the parasite in the founding human populations.85

THE AGRICULTURAL TRANSITION The process of plant and animal domestication began by 11,500 BP86 and perhaps, on a limited basis, even earlier (for example, with dogs87). This transition likely had a major effects on human-parasite coevolution – directly through close proximity to livestock, and indirectly through associated changes to a sedentary life style, higher population densities, and modifications to the environment. Whether a substantial number of modern human parasites infected our species only following the onset of agriculture88 is a matter of debate.89 Regardless, even for longstanding human parasites, ecological changes associated with the agricultural transition may have led to increased infection rates (Table 1). Consider tapeworms, which may have parasitized hominins since the Pliocene, as discussed earlier. Prior to the agricultural transition, the tapeworm lifecycle depended on the ingestion of eggs deposited with hominin feces by free-ranging herbivores, who would later need to be hunted or scavenged upon by different hominin individuals. However, following pig and cattle domestication, the tapeworm life cycle could be completed much more readily, with now sedentary humans living nearby their circumscribed and slaughter-destined livestock. Thus, tapeworm infection rates may have increased markedly. Similar arguments can be made for multiple other human parasites and the various ecological and demographic byproducts of the agricultural

transition. Increased herbivore concentrations close to human settlements may have precipitated larger local populations of the insect vectors for many human parasites, including malaria, river blindness, and sleeping sickness90,91 (see Table 1 for a list of specific parasites). Standing water habitats created for irrigation and storage likely also increased the local densities of at least some insect vectors.92 The likelihood that an individual insect would encounter multiple humans for parasite transmission during its short life span and across its necessary home range (for example,

Parasites and human evolution.

Our understanding of human evolutionary and population history can be advanced by ecological and evolutionary studies of our parasites. Many parasites...
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