Why infectious disease research needs community ecology

Johnson, Pieter T. J.; Roode, Jacobus C. de; Fenton, Andy

doi:10.1126/science.1259504

Cited by 363 publications

(380 citation statements)

References 101 publications

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“…Mixed infections represent a major problem for public health because they complicate the development of treatments and vaccines (1,4). Some pathogen strains are more infectious or do more harm to certain host species (5,6).…”

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confidence: 99%

Multistrain Infections with Lyme Borreliosis Pathogens in the Tick Vector

Durand

Herrmann

Genné

et al. 2017

Appl Environ Microbiol

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Mixed or multiple-strain infections are common in vector-borne diseases and have important implications for the epidemiology of these pathogens. Previous studies have mainly focused on interactions between pathogen strains in the vertebrate host, but little is known about what happens in the arthropod vector. Borrelia afzelii and Borrelia garinii are two species of spirochete bacteria that cause Lyme borreliosis in Europe and that share a tick vector, Ixodes ricinus. Each of these two tick-borne pathogens consists of multiple strains that are often differentiated using the highly polymorphic ospC gene. For each Borrelia species, we studied the frequencies and abundances of the ospC strains in a wild population of I. ricinus ticks that had been sampled from the same field site over a period of 3 years. We used quantitative PCR (qPCR) and 454 sequencing to estimate the spirochete load and the strain diversity within each tick. For B. afzelii, there was a negative relationship between the two most common ospC strains, suggesting the presence of competitive interactions in the vertebrate host and possibly the tick vector. The flat relationship between total spirochete abundance and strain richness in the nymphal tick indicates that the mean abundance per strain decreases as the number of strains in the tick increases. Strains with the highest spirochete load in the nymphal tick were the most common strains in the tick population. The spirochete abundance in the nymphal tick appears to be an important life history trait that explains why some strains are more common than others in nature.IMPORTANCE Lyme borreliosis is the most common vector-borne disease in the Northern Hemisphere and is caused by spirochete bacteria that belong to the Borrelia burgdorferi sensu lato species complex. These tick-borne pathogens are transmitted among vertebrate hosts by hard ticks of the genus Ixodes. Each Borrelia species can be further subdivided into genetically distinct strains. Multiple-strain infections are common in both the vertebrate host and the tick vector and can result in competitive interactions. To date, few studies on multiple-strain vector-borne pathogens have investigated patterns of cooccurrence and abundance in the arthropod vector. We demonstrate that the abundance of a given strain in the tick vector is negatively affected by the presence of coinfecting strains. In addition, our study suggests that the spirochete abundance in the tick is an important life history trait that can explain why some strains are more common in nature than others.

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mentioning

confidence: 99%

Multistrain Infections with Lyme Borreliosis Pathogens in the Tick Vector

Durand

Herrmann

Genné

et al. 2017

Appl Environ Microbiol

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“…However, we believe that this concept is not limited to the zoochlorellae-bearing symbionts but rather, may be a general phenomenon in symbiotic relationships where predation is the activating catalyst for virus production. Thus, this finding could substantially transform the understanding of virus population dynamics in complex food webs (24).…”

Section: Discussionmentioning

confidence: 87%

Predators catalyze an increase in chloroviruses by foraging on the symbiotic hosts of zoochlorellae

DeLong

Al-Ameeli

Duncan

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Virus population growth depends on contacts between viruses and their hosts. It is often unclear how sufficient contacts are made between viruses and their specific hosts to generate spikes in viral abundance. Here, we show that copepods, acting as predators, can bring aquatic viruses and their algal hosts into contact. Specifically, predation of the protistParamecium bursariaby copepods resulted in a >100-fold increase in the number of chloroviruses in 1 d. Copepod predation can be seen as an ecological “catalyst” by increasing contacts between chloroviruses and their hosts, zoochlorellae (endosymbiotic algae that live within paramecia), thereby facilitating viral population growth. When feeding, copepods passedP. bursariathrough their digestive tract only partially digested, releasing endosymbiotic algae that still supported viral reproduction and resulting in a virus population spike. A simple predator–prey model parameterized for copepods consuming protists generates cycle periods for viruses consistent with those observed in natural ponds. Food webs are replete with similar symbiotic organisms, and we suspect the predator catalyst mechanism is capable of generating blooms for other endosymbiont-targeting viruses.

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“…Recently, pioneering studies have experimentally or theoretically reported that ontogenetic functional diversity can influence ecosystem functioning more strongly than interspecific functional diversity (Rudolf and Rasmussen 2013a, b;Reichstein et al 2015), suggesting that the ontogenetic perspective is critical in ecosystem ecology. Furthermore, community ecology plays a crucial role in various applications that concern ecosystem management, such as agriculture (Gliessman 1990), fishery (Mangel and Levins 2005), epidemiology Johnson et al 2015), and biodiversity conservation under global climate change (Nakazawa and Doi 2012;Post 2013). However, these areas have not yet been fully considered from the ontogenetic perspective, except for fisheries management (Hsieh et al 2010).…”

Section: Conclusion and Future Perspectivesmentioning

confidence: 99%

Individual interaction data are required in community ecology: a conceptual review of the predator–prey mass ratio and more

Nakazawa

2016

Ecological Research

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Community ecology is traditionally speciesbased and assumes that species comprise identical individuals. However, intraspecific variation is ubiquitous in nature because of ontogenetic growth and critical in food-we dynamics. To understand individual interaction-mediated food webs, researchers have recently focused on body size as the most fundamental biological aspect and assessed a parameter called the predatorprey mass ratio (PPMR). Herein, I review the conceptual development of the PPMR and suggest four major concerns regarding its measurement: (1) PPMR should be measured at the individual level because species-averaged values distort actual feeding relationships, (2) individual-level PPMR data on gape-unconstrained predators (e.g., terrestrial carnivores) are limited because previous studies have targeted gape-limited fish predators, (3) predators' prey size selectivity (preferred PPRM) is conceptually different from dietary prey size (realized PPMR) and should be distinguished by incorporating environmental prey abundance information, and (4) determinants of preferred PPMR, rather than those of realized PPMR, should be identified to describe size-dependent predation. Future studies are encouraged to explore not only predation but also other interaction types (e.g., competition, mutualism, and herbivory) at the individual level. However, this is not likely to occur while ecological communities are still considered to be interspecific interaction networks. To resolve this situation and more comprehensively understand biodiversity and ecosystem functioning, I suggest that community ecology requires a paradigm shift in the unit of interaction from species to individuals, similar to evolutionary biology, which revolutionized the unit of selection, because interactions occur between individuals.

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Why infectious disease research needs community ecology

Cited by 363 publications

References 101 publications

Multistrain Infections with Lyme Borreliosis Pathogens in the Tick Vector

Multistrain Infections with Lyme Borreliosis Pathogens in the Tick Vector

Predators catalyze an increase in chloroviruses by foraging on the symbiotic hosts of zoochlorellae

Individual interaction data are required in community ecology: a conceptual review of the predator–prey mass ratio and more

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