How To In Host Infection Models Differ Between Animals And Humans

Abstract

Many of the major human infectious diseases, including some now bars to humans and absent from animals, are 'new' ones that arose merely later the origins of agriculture. Where did they come from? Why are they overwhelmingly of Old Earth origins? Here we testify that answers to these questions are different for tropical and temperate diseases; for instance, in the relative importance of domestic animals and wild primates as sources. We identify five intermediate stages through which a pathogen exclusively infecting animals may become transformed into a pathogen exclusively infecting humans. We propose an initiative to resolve disputed origins of major diseases, and a global early on alarm system to monitor pathogens infecting individuals exposed to wild animals.

Main

Homo hunter/gatherer populations currently suffer, and presumably have suffered for millions of years, from infectious diseases similar or identical to diseases of other wild primate populations. All the same, the about important infectious diseases of modern food-producing human populations also include diseases that could have emerged simply within the past xi,000 years, following the ascension of agriculture^1,2. We infer this because, every bit discussed below, these diseases can simply be sustained in big dense human populations that did not exist anywhere in the world before agriculture. What were the sources of our major infectious diseases, including these 'new' ones? Why practice so many animal pathogens, including virulent viruses similar Ebola and Marburg, periodically infect human hosts but and so fail to institute themselves in man populations?

A tentative earlier formulation^ane noted that major infectious diseases of temperate zones seem to have arisen overwhelmingly in the Old World (Africa, Asia and Europe), often from diseases of Old World domestic animals. Hence one goal of this commodity is to re-appraise that determination in the light of studies of the past decade. Another goal is to extend the analysis to origins of tropical diseasesⁱⁱⁱ. We shall prove that they also arose mainly in the Old World, but for dissimilar reasons, and more often than not not from diseases of domestic animals.

These results provide a framework for addressing unanswered questions about the evolution of human infectious diseases—questions not only of practical importance to physicians, and to all the rest of us as potential victims, merely also of intellectual involvement to historians and evolutionary biologists. Historians increasingly recognize that infectious diseases have had major furnishings on the course of history; for instance, on the European conquest of Native Americans and Pacific Islanders, the inability of Europeans to conquer the Old World tropics for many centuries, the failure of Napoleon'south invasion of Russia, and the failure of the French endeavour to consummate construction of a Panama Canal^4,5,six. Evolutionary biologists realize that infectious diseases, equally a leading cause of human morbidity and mortality, have exerted important selective forces on our genomes^2,7.

We begin by defining 5 stages in the evolutionary transformation of an animal pathogen into a specialized pathogen of humans, and past because why and then many pathogens fail to brand the transition from one stage to the next. Nosotros then assemble a database of 15 temperate and 10 tropical diseases of loftier evolutionary and/or historical touch, and nosotros compare their characteristics and origins. Our concluding section lays out some unresolved questions and suggests two expanded research priorities. We restrict our discussion to unicellular microbial pathogens. We exclude macroparasites (in the sense of ref. 7), likewise as normally beneficial commensals that cause serious disease simply in weakened hosts. The extensive Supplementary Information provides details and references on our 25 diseases, robustness tests of our conclusions, factors affecting transitions between affliction stages, and mod practices altering the risk of emergence of new diseases.

Evolutionary stages

Box one delineates five intergrading stages (Fig. i) through which a pathogen exclusively infecting animals (Stage 1) may go transformed into a pathogen exclusively infecting humans (Stage v). Supplementary Table S1 assigns each of the 25 major diseases discussed (Supplementary Notation S1) to one of these five stages.

Figure one: Analogy of the five stages through which pathogens of animals evolve to crusade diseases confined to humans.

(Run across Box 1 for details.) The iv agents depicted have reached different stages in the procedure, ranging from rabies (even so acquired only from animals) to HIV-1 (now acquired but from humans).

Full size paradigm

A large literature discusses the weather required for a Phase 5 epidemic to persist^2,seven. Briefly, if the disease infects only humans and lacks an animal or environmental reservoir, each infected human introduced into a big population of susceptible individuals must on average give rise during his/her contagious lifespan to an infection in at to the lowest degree ane other individual. Persistence depends on factors such every bit the elapsing of a host's infectivity; the rate of infection of new hosts; rate of development of host protective immunity; and host population density, size and construction permitting the pathogen'due south regional persistence despite temporary local extinctions.

Less well understood are two of the disquisitional transitions between stages, discussed in Box 2. One is the transition from Phase 1 to Stage 2, when a pathogen initially bars to animals showtime infects humans. The other is the transition from Stage two to Stages three and 4 (run into also Supplementary Note S2), when a pathogen of animal origin that is nevertheless transmissible to humans evolves the power to sustain many cycles of human being-to-human being transmission, rather than merely a few cycles earlier the outbreak dies out (equally seen in modern Ebola outbreaks).

Database and conclusions

Database

Supplementary Table S1 lists x characteristics for each of 25 important 'temperate' (fifteen) and 'tropical' (10) diseases (meet Supplementary Notation S3 for details of this stardom). Our aim was to select well-divers diseases causing the highest mortality and/or morbidity and hence of the highest historical and evolutionary significance (see Supplementary Note S1 for details of our pick criteria). Of the 25 diseases, nosotros selected 17 because they are the ones assessed by ref. 8 as imposing the heaviest world burdens today (they have the highest disability-adjusted life years (DALY) scores). Of the 17 diseases, 8 are temperate (hepatitis B, influenza A, measles, pertussis, rotavirus A, syphilis, tetanus and tuberculosis), and 9 are tropical (acquired allowed deficiency syndrome (AIDS), Chagas' affliction, cholera, dengue haemorrhagic fever, East and West African sleeping sicknesses, falciparum and vivax malarias, and visceral leishmaniasis). We selected eight others (temperate diphtheria, mumps, plague, rubella, smallpox, typhoid and typhus, plus tropical yellow fever) because they imposed heavy burdens in the by, although modern medicine and public health have either eradicated them (smallpox) or reduced their burden. Except for AIDS, dengue fever, and cholera, which have spread and attained global impact in modern times, most of these 25 diseases have been important for more than two centuries.

Are our conclusions robust to variations in these selection criteria? For about a dozen diseases with the highest modern or historical burdens (for case, AIDS, malaria, plague, smallpox), there tin be lilliputian doubt that they must be included, simply one could debate some of the next choices. Hence we drew up three culling sets of diseases sharing a get-go list of 16 indisputable major diseases but differing in the next choices, and we performed all 10 analyses described below on all iii sets. It turned out that, with one pocket-size exception, the three sets yielded qualitatively the aforementioned conclusions for all x analyses, although differing in their levels of statistical significance (run into Supplementary Note S4). Thus, our conclusions do seem to be robust.

Temperate/tropical differences

Comparisons of these temperate and tropical diseases yield the post-obit conclusions:

• A higher proportion of the diseases is transmitted past insect vectors in the tropics (viii/10) than in the temperate zones (2/15) (P < 0.005, χ ⁱⁱ-test, degrees of freedom, d.f. = ane). This difference may be partly related to the seasonal cessations or declines of temperate insect activeness.

• A higher proportion (P = 0.009) of the diseases conveys long-lasting immunity (xi/15) in the temperate zones than in the tropics (two/10).

• Beast reservoirs are more than frequent (P < 0.005) in the tropics (8/x) than in the temperate zones (3/15). The deviation is in the contrary direction (P = 0.1, NS, not significant) for environmental reservoirs (ane/10 versus 6/15), but those environmental reservoirs that do be are generally not of major significance except for soil bearing tetanus spores.

• Near of the temperate diseases (12/15) are acute rather than wearisome, chronic, or latent: the patient either dies or recovers within ane to several weeks. Fewer (P = 0.01) of the tropical diseases are astute: 3/10 terminal for one or two weeks, 3/10 final for weeks to months or years, and 4/10 last for many months to decades.

• A somewhat college proportion of the diseases (P = 0.08, NS) belongs to Stage 5 (strictly confined to humans) in the temperate zones (10/15 or eleven/fifteen) than in the torrid zone (three/10). The paucity of Phase 2 and Stage 3 diseases (a full of but 5 such diseases) on our listing of 25 major human diseases is noteworthy, because some Phase two and Stage iii pathogens (such as anthrax and Ebola) are notoriously virulent, and because theoretical reasons are often avant-garde (only also denied) as to why Stage 5 microbes with long histories of adaptation to humans should tend to evolve low morbidity and mortality and not cause major diseases. We hash out explanations for this outcome in Supplementary Notation S5.

About (x/xv) of the temperate diseases, but none of the tropical diseases (P < 0.005), are so-chosen 'crowd epidemic diseases' (asterisked in Supplementary Tabular array S1), defined equally ones occurring locally every bit a brief epidemic and capable of persisting regionally merely in large human populations. This difference is an immediate issue of the differences enumerated in the preceding five paragraphs. If a disease is astute, efficiently transmitted, and quickly leaves its victim either dead or else recovering and immune to re-infection, the epidemic before long exhausts the local pool of susceptible potential victims. If in addition the disease is bars to humans and lacks significant brute and ecology reservoirs, depletion of the local pool of potential victims in a small, thin man population results in local termination of the epidemic. If, nevertheless, the human being population is large and dense, the illness can persist past spreading to infect people in adjacent areas, and then returning to the original area in a later twelvemonth, when births and growth have regenerated a new ingather of previously unexposed non-immune potential victims. Empirical epidemiological studies of illness persistence or disappearance in isolated human populations of various sizes have yielded estimates of the population required to sustain a oversupply disease: at least several hundred thousand people in the cases of measles, rubella and pertussis^2,vii. But man populations of that size did not be anywhere in the globe until the steep rising in human numbers that began around 11,000 years ago with the development of agriculture^1,ix. Hence the crowd epidemic diseases of the temperate zones must have evolved since then.

Of form, this does not hateful that human hunter/gatherer communities lacked infectious diseases. Instead, like the thin populations of our primate relatives, they suffered from infectious diseases with characteristics permitting them to persist in pocket-sized populations, dissimilar crowd epidemic diseases. Those characteristics include: occurrence in animal reservoirs as well as in humans (such as yellow fever); incomplete and/or non-lasting immunity, enabling recovered patients to remain in the pool of potential victims (such every bit malaria); and a slow or chronic class, enabling individual patients to continue to infect new victims over years, rather than for only a week or two (such every bit Chagas' illness).

Pathogen origins

(See details for each affliction in Supplementary Note S10). Current information suggests that 8 of the 15 temperate diseases probably or perhaps reached humans from domestic animals (diphtheria, influenza A, measles, mumps, pertussis, rotavirus, smallpox, tuberculosis); three more probably reached u.s.a. from apes (hepatitis B) or rodents (plague, typhus); and the other four (rubella, syphilis, tetanus, typhoid) came from withal-unknown sources (run across Supplementary Note S6). Thus, the ascent of agriculture starting xi,000 years ago played multiple roles in the development of brute pathogens into homo pathogens^i,4,10. Those roles included both generation of the large man populations necessary for the evolution and persistence of human crowd diseases, and generation of large populations of domestic animals, with which farmers came into much closer and more than frequent contact than hunter/gatherers had with wild animals. Moreover, as illustrated by influenza A, these domestic animal herds served as efficient conduits for pathogen transfers from wild animals to humans, and in the process may have evolved specialized crowd diseases of their own.

Information technology is interesting that fewer tropical than temperate pathogens originated from domestic animals: not more than than iii of the ten tropical diseases of Supplementary Tabular array S1, and maybe none (see Supplementary Note S7). Why practise temperate and tropical human diseases differ and so markedly in their brute origins? Many (4/x) tropical diseases (AIDS, dengue fever, vivax malaria, yellow fever) but merely i/15 temperate diseases (hepatitis B) have wild non-human primate origins (P = 0.04). This is because although not-human primates are the animals most closely related to humans and hence pose the weakest species barriers to pathogen transfer, the vast bulk of primate species is tropical rather than temperate. Conversely, few tropical but many temperate diseases arose from domestic animals, and this is because domestic animals live mainly in the temperate zones, and their concentration there was formerly even more lop-sided (encounter Supplementary Note S8).

A final noteworthy point about animal-derived homo pathogens is that virtually all arose from pathogens of other warm-blooded vertebrates, primarily mammals plus in two cases (influenza A and ultimately falciparum malaria) birds. This comes as no surprise, considering the species barrier to pathogen transfer posed by phylogenetic distance (Box 2). An expression of this barrier is that primates constitute simply 0.v% of all vertebrate species but accept contributed nearly twenty% of our major homo diseases. Expressed in another fashion, the number of major human diseases contributed, divided by the number of beast species in the taxonomic group contributing those diseases, is approximately 0.ii for apes, 0.017 for non-human primates other than apes, 0.003 for mammals other than primates, 0.00006 for vertebrates other than mammals, and either 0 or else 0.000003 (if cholera really came from aquatic invertebrates) for animals other than vertebrates (see Supplementary Annotation S9).

Geographic origins

To an overwhelming caste, the 25 major human pathogens analysed here originated in the Old World. That proved to be of great historical importance, because it facilitated the European conquest of the New Globe (the Americas). Far more Native Americans resisting European colonists died of newly introduced Old World diseases than of sword and bullet wounds. Those invisible agents of New Earth conquest were Old Globe microbes to which Europeans had both some caused amnesty based on individual exposure and some genetic resistance based on population exposure over fourth dimension, but to which previously unexposed Native American populations had no immunity or resistance^1,iv,5,six. In contrast, no comparably devastating diseases awaited Europeans in the New World, which proved to be a relatively salubrious environment for Europeans until yellow fever and malaria of Old World origins arrived^eleven.

Why was pathogen substitution between Quondam and New Worlds so diff? Of the 25 major human diseases analysed, Chagas' disease is the just one that conspicuously originated in the New Globe. For ii others, syphilis and tuberculosis, the debate is unresolved: it remains uncertain in which hemisphere syphilis originated, and whether tuberculosis originated independently in both hemispheres or was brought to the Americas by Europeans. Zip is known near the geographic origins of rotavirus, rubella, tetanus and typhus. For all of the other 18 major pathogens, Old World origins are certain or likely.

Our preceding discussion of the brute origins of human pathogens may help explain this asymmetry. More temperate diseases arose in the Old Globe than New Earth considering far more animals that could replenish ancestral pathogens were domesticated in the Erstwhile World. Of the world'due south fourteen major species of domestic mammalian livestock, 13, including the 5 most abundant species with which we come into closest contact (moo-cow, sheep, goat, sus scrofa and horse), originated in the Old Worldⁱ. The sole livestock species domesticated in the New Globe was the llama, but it is non known to take infected u.s. with any pathogens^i,ii—mayhap because its traditional geographic range was bars to the Andes, information technology was not milked or ridden or hitched to ploughs, and it was not cuddled or kept indoors (as are some calves, lambs and piglets). Among the reasons why far more tropical diseases (nine versus 1) arose in the Sometime World than the New World are that the genetic distance between humans and New Earth monkeys is almost double that betwixt humans and Onetime World monkeys, and is many times that between humans and Old Earth apes; and that much more than evolutionary time was bachelor for transfers from animals to humans in the Old World (near 5 million years) than in the New World (about 14,000 years).

Outlook and hereafter research directions

Many research directions on infectious disease origins merit more try. We conclude by calling attention to two such directions: clarifying the origins of existing major diseases, and surveillance for early detection of new potentially major diseases.

Origins of established diseases

This review illustrates big gaps in our agreement of the origins of even the established major infectious diseases. Near all the studies that we have reviewed were based on specimens nerveless opportunistically from domestic animals and a few easily sampled wild animal species, rather than on systematic surveys for particular classes of agents over the spectrum of domestic and wild animals. A case in bespeak is our ignorance even about smallpox virus, the virus that has had perhaps the greatest impact on human history in the by iv,000 years. Despite some knowledge of poxviruses infecting our domestic mammals, we know little almost poxvirus diverseness among African rodents, from which those poxviruses of domestic mammals are thought to take evolved. Nosotros do non fifty-fifty know whether 'camelpox', the closest known relative of smallpox virus, is truly bars to camels as its name implies or is instead a rodent virus with a broad host range. At that place could be still-unknown poxviruses more similar to smallpox virus in yet unstudied animal reservoirs, and those unknown poxviruses could be of import not but as illness threats only also every bit reagents for drug and vaccine evolution.

As basic questions arise for other major pathogens. While falciparum malaria, an infection imposing ane of the heaviest global burdens today, seems to have originated from a bird parasite whose descendants include both the Plasmodium falciparum infecting humans and the P. reichenowii infecting chimpanzees, malaria researchers all the same debate whether the bird parasite was introduced to both humans and chimpanzees¹² a few m years ago in clan with human agriculture, or instead more than v meg years agone before the split of humans and chimpanzees from each other^xiii. Although resolving this debate will not help us eradicate malaria, it is fascinating in its own right and could contribute to our broader agreement of disease emergence. In the case of rubella, a human crowd disease that must take emerged only in the past 11,000 years and for which some shut relative may thus all the same exist among animals, no even remotely related virus is known; ane or more may be lurking undiscovered somewhere. Does the recent identification of porcine rubulavirus and the Mapuera virus in bats as the closest known relatives of mumps virus mean that pigs infected humans, or that man mumps infected pigs, or that bats independently infected both humans and pigs? Is human being tuberculosis descended from a ruminant mycobacterium that recently infected humans from domestic animals (a formerly prevalent view), or from an aboriginal human mycobacterium that has come up to infect domestic and wild ruminants (a currently pop view)?

To fill up these and other yawning gaps in our understanding of illness origins, we propose an 'origins initiative' aimed at identifying the origins of a dozen of the nigh important man infectious diseases: for example, AIDS, cholera, dengue fever, falciparum malaria, hepatitis B, influenza A, measles, plague, rotavirus, smallpox, tuberculosis and typhoid. Although more than is already known about the origins of some of these agents (AIDS, influenza A and measles) than about others (rotavirus, smallpox and tuberculosis), more comprehensive screening is still likely to yield significant new data about fifty-fifty the most studied agents, equally illustrated past the recent demonstration that gorillas rather than chimpanzees were probably the donor species for the O-group of human immunodeficiency virus (HIV)-1^xiv. The proposed effort would involve systematic sampling and phylogeographic analysis of related pathogens in diverse brute species: not just pigs and other species chosen for their set availability, but a wider range of wild and domestic species whose direct contact (for instance, every bit bushmeat) or indirect contact (for case, vector-mediated) with humans could plausibly have led to human infections. In addition to the historical and evolutionary significance of knowledge gained through such an origins initiative, it could yield other benefits such as: identifying the closest relatives of man pathogens; a improve agreement of how diseases take emerged; new laboratory models for studying public wellness threats; and mayhap clues that could aid in predictions of future disease threats.

A global early warning arrangement

Most major human being infectious diseases accept brute origins, and we continue to be bombarded past novel animal pathogens. Yet at that place is no ongoing systematic global attempt to monitor for pathogens emerging from animals to humans. Such an effort could help us to depict the diversity of microbial agents to which our species is exposed; to narrate animal pathogens that might threaten the states in the time to come; and perchance to detect and control a local human being emergence before it has a chance to spread globally.

In our view, monitoring should focus on people with high levels of exposure to wild animals, such as hunters, butchers of wild game, wildlife veterinarians, workers in the wildlife trade, and zoo workers. Such people regularly go infected with fauna viruses, and their infections tin can be monitored over fourth dimension and traced to other people in contact with them. 1 of u.s. (N.D.W.) has been working in Cameroon to monitor microbes in people who chase wild game, in other people in their community, and in their animal prey^fifteen. The study is now expanding to other continents and to monitor domestic animals (such every bit dogs) that live in close proximity to humans but are exposed to wild animals through hunting and scavenging. Monitoring of people, animals, and animal die-offs^xvi will serve as an early warning organisation for disease emergence, while besides providing a unique archive of pathogens infecting humans and the animals to which we are exposed. Specimens from such highly exposed human populations could be screened specifically for agents known to be present in the animals they hunt (for example, retroviruses among hunters of non-human primates), likewise equally generically using wide screening tools such as viral microarrays¹⁷ and random amplification polymerase concatenation reaction (PCR)^xviii. Such monitoring efforts besides provide potentially invaluable repositories, which would be available for study after future outbreaks in society to reconstruct an outbreak'south origin, and equally a source of relevant reagents.

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Acknowledgements

Nosotros thank L. Krain for assistance with Supplementary Notation S10; 1000. Antolin, D. Burke, L. Fleisher, E. Holmes, Fifty. Real, A. Rimoin, R. Weiss and One thousand. Woolhouse for comments; and many other colleagues for providing data. This piece of work was supported by an NIH Director'south Pioneer Award and Fogarty International Center IRSDA Laurels (to North.D.W.), a Due west. W. Smith Foundation award (to Due north.D.Westward.), and National Geographic Society awards (to J.D. and Northward.D.Westward.).

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Authors and Affiliations

1. Department of Epidemiology, School of Public Wellness, University of California, Los Angeles 90095-1772, USA

   Nathan D. Wolfe

2. Division of Infectious Diseases, David Geffen School of Medicine, University of California, Los Angeles 90095-1688, Us

   Claire Panosian Dunavan

3. Departments of Geography and of Environmental Health Sciences, University of California, Los Angeles 90095-1524, The states

   Jared Diamond

Corresponding authors

Correspondence to Nathan D. Wolfe or Jared Diamond.

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Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

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Wolfe, N., Dunavan, C. & Diamond, J. Origins of major human infectious diseases. Nature 447, 279–283 (2007). https://doi.org/ten.1038/nature05775

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• Received: 08 September 2006

• Accustomed: 22 March 2007

• Issue Date: 17 May 2007

• DOI : https://doi.org/10.1038/nature05775

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