Applying the Theory of Island Biogeography to Emerging Pathogens: Toward Predicting the Sources of Future Emerging Zoonotic and Vector-Borne Diseases

Abstract

Emerging infectious diseases are recognized as increasing threats to public and animal health, global economy, and social and political stability. Climate change, environmental changes, changes in human demographics and behaviors, and the rise of global trade and travel are most-often-cited drivers for the emergence of infectious diseases in human and animal populations (Schrag and Wiener 1995, Daszak et al. 2001, Dobson and Foufopoulos 2001, May et al. 2001, Taylor et al. 2001, Antia et al. 2003, IOM 2003, Kuiken et al. 2003, Weiss and McMichael 2004, Wolfe et al. 2005, Woolhouse and Gowtage-Sequeria 2005, Chomel et al. 2007, Woolhouse and Gaunt 2007, Jones et al. 2008). Emerging pathogens are more likely to be zoonotic or vector-borne with a broad host range (Daszak et al. 2000, Taylor et al. 2001, Woolhouse and Gowtage-Sequeria 2005, Jones et al. 2008). Emerging pathogens are also more frequently RNA viruses (Woolhouse and Gowtage-Sequeria 2005), which may better adapt to and establish in novel host species (Antia et al. 2003, Andre and Day 2005, Woolhouse et al. 2005). Determining the factors driving disease emergence eventually aims at assisting the prediction of the future emergence of infectious diseases. However, because of the multifactorial nature of the drivers involved (IOM 2003), our ability to predict which pathogens may arise in human or animal populations in the future remains limited (WHO/FAO/OIE 2004). In particular, the ability to identify the animal reservoirs where the greatest risks to human health will originate was deemed improbable (WHO/FAO/OIE 2004). Applying the theory of island biogeography (MacArthur and Wilson 1967) to emerging pathogens identifies (i) interactions between recipient host species and species sources of pathogens (including vector species), (ii) interactions within species sources of pathogens, and (iii) interactions within recipient host species, as mechanisms directly driving disease emergence. Most identified drivers for disease emergence correspond to changes in one or more of these three sets of interactions. Importantly, applying the theory of island biogeography to emerging pathogens assists in predicting from which animal species future zoonotic and vector-borne pathogens will most probably emerge. Identifying known and unknown pathogens such species harbor may bring us one step forward toward predicting which pathogen will next emerge in human populations.

A n emerging pathogen can be defined as the causative agent of an infectious disease whose incidence is increasing (Woolhouse et al. 2005). Emerging pathogens include pathogens unable to transmit between individuals of the recipient host species but repeatedly introduced from a known or unknown source (basic reproductive number, as the average number of secondary infections arising from one infected individual in a susceptible host population, R ₀ = 0 in the recipient host species, e.g., Echinococcus multilocularis); pathogens that can transmit between individuals of the recipient host species but for which chains of transmission are self-limited (0 < R ₀ < 1, e.g., Nipah virus); and pathogens that can transmit between individuals of the recipient host species and for which chains of transmission result in an epidemic spread of the disease (R ₀ > 1, e.g., SARS coronavirus) (Wolfe et al. 2007, Woolhouse and Gaunt 2007). Disease emergence thus can result from an increase in the frequency of introductions of the pathogen into the recipient host species (with no change in R ₀), or from an increase in its host-to-host transmission within the recipient host species (associated with an increase in R ₀).

Hosts can be considered as islands for pathogens (Kuris et al. 1980)—islands that can successfully be colonized provided that introduced pathogens are able to establish (cause infection) and avoid extinction (transmit between hosts) (May et al. 2001). The analogy of hosts as islands for pathogens was proposed after MacArthur and Wilson's theory of island biogeography, a landmark contribution to ecology (MacArthur and Wilson 1967). Biogeography is the study of the distribution of biodiversity, which can be measured by species richness (number of species), over space and time. MacArthur and Wilson (1967) proposed that a biotic equilibrium of the number of species on a given island is reached when the immigration and extinction rates (species/unit time) equal each other (Fig. 1). Immigration rates fall and extinction rates rise with the number of species present on the island. Immigration rates also fall when the degree of isolation from the source regions that supply the species (source-island distance) is increased; extinction rates also rise when the area of the island is decreased (Fig. 1). Likewise, it was proposed that parasite species richness results from the balance of rates of parasite colonization and extinction (Poulin 2004) (Fig. 1). Source-island distance–like factors may influence the rate of parasite colonization, and relate to interactions between sources of parasites and recipient hosts, mostly through spatial or behavioral overlap (e.g., host habitat and geographical ranges, and diet). Island area–like factors may influence the rate of parasite extinction, and include species–area relationships (through host body size and lifespan) but also relate to intraspecific interactions of the newly colonized hosts (through population density and social behavior) (Kuris et al. 1980) (for a review, see Poulin, 2004).

FIG. 1.

Equilibrium models of species richness on islands (black and bold text) and of parasite species richness within host species (gray and nonbold text). S, number of species at equilibrium; X, species turnover rate at equilibrium. Adapted from MacArthur and Wilson (1967).

Changes in source-island distance–like factors and island area–like factors (i.e., changes in the degree of interactions between recipient host species and species source of pathogens, and changes in the degree of interactions within recipient host species) resulting in changes in rates of pathogen colonization and/or extinction may explain the increase in the number of novel pathogens in human (or animal) populations (Fig. 2). Indeed, most identified drivers for disease emergence in human populations correspond to changes in one or both sets of interactions (Table 1). Thus, economic development and the rise of bushmeat hunting in Africa and Asia, or changes in land use and the conversion of natural habitats into agricultural lands in South America, have reduced source-island distances between animal species sources of pathogens and humans, and contributed to the introduction of emerging pathogens into human populations, for example, human immunodeficiency viruses (HIV), filoviruses, monkeypox virus, Severe Acute Respitory Syndrome (SARS) coronavirus, or New World arenaviruses (Charrel and Lamballerie 2003, Wolfe et al. 2005, Chomel et al. 2007). Urbanization, global travel, and changes in human demographics and behaviors have facilitated contact between humans, and increased island area, contributing to the establishment and spread of emerging pathogens, for example, urban strains of dengue and yellow fever viruses, HIV, or SARS coronavirus (Yuill 1986, May et al. 2001, Anderson et al. 2004).

FIG. 2.

Illustration of the process of disease emergence based on the theory of island biogeography applied to the transmission of pathogens to novel host species.

Table 1.

Institute of Medicine (IOM) Ecological Drivers for Emergence of Infectious Diseases (IOM 2003) and Corresponding Drivers Based on the Island Biogeography Framework for Disease Emergence, for Selected Examples of Significant Emerging Infectious Diseases in Humans

IOM list of drivers for emergence	Examples	Island biogeography framework for disease emergence
Microbial adaptation and change	Acquisition of specific mutations that increased R ₀ in humans and emergence of SARS coronavirus (Song et al. 2005)	[Nonecological driver for emergence: intrinsic characteristics of pathogens]
Human susceptibility to infection	Immunodeficiency and emergence of opportunistic pathogens (Kaplan et al. 1998)	Island-area-like factor
Climate and weather	Increase in population size/density of source species associated with El Nino events or global warming, for example, rodents and arthropod vectors and emergence of Sin nombre virus and European tick-borne encephalitis virus (Engelthaler et al. 1999, Randolph 2001)	Source-area–like factors
Changing ecosystems	Reforestation and increase in population size/density of source species, for example, deer and tick populations and emergence of Borrelia burgdorferi (Barbour and Fish 1993)	Source-area–like factors
Human demographics and behavior	Behavioral changes leading to increased contact rates with infected humans, and emergence of HIV (May et al. 2001), SARS coronavirus (Chomel et al. 2007), and yellow fever virus, dengue virus, and Chickungunya virus (Yuill 1986)	Island-area-like factors
Economic development and land use	Deforestation, rise in bushmeat hunting, and increase in population size/density of source or stepping-stone species, for example, primates, rodents, small carnivores, and emergence of HIV, filoviruses, monkeypox virus, SARS coronavirus (Wolfe et al. 2005, Chomel et al. 2007). Deforestation, agricultural development, and increase in population size/density of source species in agricultural lands, for example, rodents and emergence of New World arenaviruses (Charrel and Lamballerie 2003); bats and emergence of Nipah virus and menangle virus (Field et al. 2001) Urbanization and associated increase in population size/density of source species in residential and urban areas, for example, bats and emergence of Australian bat lyssavirus and hendra virus (Field et al. 2001); arthropod vectors and emergence of dengue virus, yellow fever virus, and Chickungunya virus (Yuill 1986) Dam building and associated increase in population size/density of source species, for example, snails and emergence of Schistosoma spp. (IOM 2003); arthropod vectors and emergence of Japanese encephalitis virus, and Rift Valley fever virus (IOM 2003)	Source-island distance–like factors Source-area–like factors
International travel and commerce	Movement of humans increasing contact rates and emergence of HIV, SARS coronavirus, Chickungunya virus, dengue virus, yellow fever virus (Yuill 1986, May et al. 2001, Anderson et al. 2004) Animal trade and movement of source species increasing interactions between source species and humans, and within source species, for example, rodents and small carnivores, and emergence of monkeypox virus, SARS coronavirus (CDC 2003; Chomel et al. 2007); arthropod vectors notably Aedes spp. and emergence of yellow fever virus and other vector-borne diseases worldwide (IOM 2003)	Island area-like factors Source-island distance–like factors Source-area–like factors
Technology and industry	Use of anti-microbial drugs and emergence of drug-resistant pathogen variants (IOM 2003)	[Nonecological driver for emergence: intrinsic characteristics of pathogens]
	Increased density of swine and poultry, and emergence of avian influenza viruses (Webster and Hulse 2004)	Source-island distance–like factorsSource-area–like factors
Breakdown of public health measuresPoverty and social inequalityWar and famineLack of political will	Decreased control of source species populations, for example, rodents and arthropod vectors and emergence of Yersinia pestis, dengue virus, and yellow fever virus (IOM 2003)Malnutrition, poor preventive education, inadequate treatment or vaccination regimes, and emergence of HIV-1, dengue virus, yellow fever virus, poliovirus, and Mycobacterium tuberculosis (IOM 2003)	Source-island distance–like factorsSource-area–like factorsIsland area-like factors

Importantly, MacArthur and Wilson (1967) demonstrated that source area and distance to the recipient island were also major source factors influencing the rate of propagules leaving the source regions and the probability for these propagules to reach the recipient island, respectively. Changes in source-area–like factors and source-island distance–like factors (i.e., changes in the degree of interactions within species sources of pathogens, and changes in the degree of interactions between species sources of pathogens and recipient host species) are thus likely to influence the rate and probability of successful cross-species transmission of pathogens (Fig. 2). Accordingly, the rise of agriculture and domestication, around 10,000 years ago, resulted in dense animal populations (large source area) in close contact with humans (short distance to recipient island) that contributed to the emergence of most pathogens now long restricted to the human species (Wolfe et al. 2007). Likewise, destruction of natural habitats in Australasia has led fruit-eating bats to colonize anthropogenic environments, reducing source-island distances between bats and humans, and favoring the emergence of Australian bat lyssavirus, menangle virus, and henipaviruses (Field et al. 2001). In addition, animal species that exploit anthropogenic environments (reducing source-island distances) typically reach higher densities than in natural environments (McKinney 2002), resulting in an increase in source area. For example, colonization of residential areas by white-tailed deer (Odocoileus virginianus) in the eastern United States is accompanied by an increase in their density and the density of tick vectors, and is associated with the emergence of Borrelia burgdorferi (Barbour and Fish 1993). Climate change or global trade also may result in expanding populations and/or increasing densities of source species, contributing to the emergence of pathogens; for example, Sin Nombre virus associated with higher density of its rodent reservoir due to El Nino events (Engelthaler et al. 1999) and European tick-borne encephalitis virus associated with increasing populations of tick vectors partly due to rising temperatures (Randolph 2001), or monkeypox virus in the United States associated with the importation of exotic pets (CDC 2003) and yellow fever virus and other vector-borne pathogens transmitted by Aedes spp. that are disseminated around the world via shipping (IOM 2003) (Table 1).

MacArthur and Wilson (1967) also demonstrated that the presence of one stepping-stone connecting the source region to a recipient island can significantly enhance immigration to the recipient island, provided that the stepping-stone is able to support populations of the immigrating species in the first place. The larger and closer is the stepping-stone to the recipient island, the greater is the increase in the immigration rate. Domestic animals have been implicated as relay species in the transmission of zoonotic pathogens from wildlife species to humans, for example, horses and swine and transmission of menangle virus and henipaviruses originating from fruit bats (Field et al. 2001), or swine and poultry and transmission of avian influenza viruses (Webster and Hulse 2004). Because of close contact with both humans and wildlife species, and increasing populations worldwide, domestic animals are likely to be major stepping-stone species favoring the emergence of infectious diseases in humans. Wildlife species also have played the role of relay in the cross-species transmission of pathogens, for example, primates and transmission of filoviruses (Wolfe et al. 2005), prairie dogs (Cynomys spp.) and transmission of monkeypox virus (CDC 2003), or palm civets (Paguma spp.) and transmission of SARS coronavirus (Chomel et al. 2007).

Surveillance of animal populations and identification of known and unknown pathogens they harbor are urged in our efforts to mitigate the effects of infectious diseases that will emerge in the future (Daszak et al. 2000, 2001, Dobson 2005, Kuiken et al. 2005, Jones et al. 2008). However, animal populations to be targeted by such surveillance efforts are rarely clearly specified. Applying the theory of island biogeography (MacArthur and Wilson 1967) to emerging pathogens identifies (i) interactions between recipient host species and species sources of pathogens (including vector species), (ii) interactions within species sources of pathogens, and (iii) interactions within recipient host species as mechanisms directly driving disease emergence. Most identified drivers for disease emergence correspond to changes in one or more of these three sets of interactions. This highlights the role not only changes in the ways recipient host species, interact with their environment and with each other, but also changes in the ways species sources of pathogens interact with their environment and with each other, play in the emergence of infectious diseases (Fig. 2). Therefore, animal species, including vector species, associated with humans and/or with expanding or growing populations at the interface of natural and human habitats (short source-island distances and large source area) should be targeted by active surveillance efforts. These species include mostly (i) domestic and laboratory animals, (ii) animals from pet trade and meat markets, (iii) the so-called pest species and managed game species, which dwell in cultures and recreational areas, and (iv) the so-called urban adapters and exploiters (McKinney 2002), which dwell in urbanized environments. A scaling system designed to assess the extent of the three sets of interactions within and between candidate source species (including vector species) and humans may help identify species with highest risk for cross-species transmission of pathogens. These species are most likely to be the sources of future emerging vector-borne and zoonotic diseases.

Footnotes

Acknowledgments

I warmly thank Andy Dobson, Penelope Koraka, Thijs Kuiken, Byron Martina, and Ab Osterhaus for fruitful discussions and useful input.

Disclosure Statement

No competing financial interests exist.

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