Vacated niches, competitive release and the community ecology of pathogen eradication

Abstract

A recurring theme in the epidemiological literature on disease eradication is that each pathogen occupies an ecological niche, and eradication of one pathogen leaves a vacant niche that favours the emergence of new pathogens to replace it. However, eminent figures have rejected this view unequivocally, stating that there is no basis to fear pathogen replacement and even that pathogen niches do not exist. After exploring the roots of this controversy, I propose resolutions to disputed issues by drawing on broader ecological theory, and advance a new consensus based on robust mechanistic principles. I argue that pathogen eradication (and cessation of vaccination) leads to a 'vacated niche', which could be re-invaded by the original pathogen if introduced. Consequences for other pathogens will vary, with the crucial mechanisms being competitive release, whereby the decline of one species allows its competitors to perform better, and evolutionary adaptation. Hence, eradication can cause a quantitative rise in the incidence of another infection, but whether this leads to emergence as an endemic pathogen depends on additional factors. I focus on the case study of human monkeypox and its rise following smallpox eradication, but also survey how these ideas apply to other pathogens and discuss implications for eradication policy.

Keywords: competitive release; ecological niche; emerging infectious disease; monkeypox; pathogen eradication; zoonosis.

Figure 1.

Monkeypox incidence and smallpox vaccine coverage, by age class, for two periods of intensified surveillance in the Kole health zone of the Democratic Republic of Congo. The per capita incidence within an age class varies inversely with the proportion of the population that has ever received the smallpox vaccine. Smallpox vaccination was officially discontinued in 1980 (a), so the continued protection in 2005–2007 (b) shows that the smallpox vaccine gives lasting immunity against clinical monkeypox infection. The overall fraction of the population that is unvaccinated is rising with time since smallpox eradication, causing a rise in monkeypox incidence. Data re-plotted from Rimoin et al. [13]; and error bars show 95% CIs.

Figure 2.

Schematic of the niche relationships of smallpox (SPX) and monkeypox (MPX) in the resource space defined by susceptible human hosts and susceptible rodents. Solid lines show the zero-net-growth isoclines (ZNGIs) for each disease, as described in the text. The dashed line shows the ZNGI for monkeypox spreading only among humans. The area outside the ZNGIs (further from the origin) represents the fundamental niche for each pathogen–host combination. The points depict four different scenarios: A, a rural village in DRC at the height of the smallpox eradication campaign; B, a rural village where the population is naive to orthopoxvirus infection (i.e. after vaccination coverage has reduced to zero); C, a high-density urban setting with an orthopoxvirus-naive human population; D, a high-density setting without monkeypox-susceptible rodents. Note that both C and D fall within the fundamental niche for monkeypox transmission in humans only.