Species’ life-history traits explain interspecific variation in reservoir competence: a possible mechanism underlying the dilution effect.
Abstract: Hosts species for multi-host pathogens show considerable variation in the species' reservoir competence, which is usually used to measure species' potential to maintain and transmit these pathogens. Although accumulating research has proposed a trade-off between life-history strategies and immune defences, only a few studies extended this to host species' reservoir competence. Using a phylogenetic comparative approach, we studied the relationships between some species' life-history traits and reservoir competence in three emerging infectious vector-borne disease systems, namely Lyme disease, West Nile Encephalitis (WNE) and Eastern Equine Encephalitis (EEE). The results showed that interspecific variation in reservoir competence could be partly explained by the species' life histories. Species with larger body mass (for hosts of Lyme disease and WNE) or smaller clutch size (for hosts of EEE) had a lower reservoir competence [corrected]. Given that both larger body mass and smaller clutch size were linked to higher extinction risk of local populations, our study suggests that with decreasing biodiversity, species with a higher reservoir competence are more likely to remain in the community, and thereby increase the risk of transmitting these pathogens, which might be a possible mechanism underlying the dilution effect.
Publication Date: 2013-01-24 PubMed ID: 23365661PubMed Central: PMC3554779DOI: 10.1371/journal.pone.0054341Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.
This research investigates the relationship between species’ life traits and their potential to carry and transmit diseases, offering insights on biodiversity loss and the resulting increase in disease transmission risk.
Research Background
- The primary focus of the study is the interspecific variation in reservoir competence, which signifies the potential of a species to maintain and transmit pathogens. This is especially important for pathogens that can infect multiple host species.
- There has been previous research suggesting a trade-off between life-history strategies and immune defences. However, very few studies have attempted to correlate this with reservoir competence.
Methodology
- The researchers used a phylogenetic comparative method to study the relationship between a species’ life-history traits and their reservoir competence.
- The study includes three emerging infectious vector-borne disease systems: Lyme disease, West Nile Encephalitis (WNE), and Eastern Equine Encephalitis (EEE).
Findings
- The study found that there is indeed a correlation between species life-history traits and reservoir competence.
- Species with a larger body mass, which are hosts for Lyme disease and WNE, or those with a smaller clutch size (the number of offspring produced at a time), which are EEE hosts, demonstrated a lower reservoir competence.
- These traits – larger body mass and smaller clutch size – are linked to a higher risk of extinction for local populations.
Implications
- The research suggests that as biodiversity decreases, species with higher reservoir competence are likely to remain, thereby increasing the risk of transmitting these pathogens.
- This suggested mechanism may underlie the “dilution effect”, which proposes that a decrease in biodiversity can lead to an increase in disease transmission.
Cite This Article
APA
Huang ZY, de Boer WF, van Langevelde F, Olson V, Blackburn TM, Prins HH.
(2013).
Species’ life-history traits explain interspecific variation in reservoir competence: a possible mechanism underlying the dilution effect.
PLoS One, 8(1), e54341.
https://doi.org/10.1371/journal.pone.0054341 Publication
Researcher Affiliations
- Resource Ecology Group, Wageningen University, Wageningen, The Netherlands. zheng.huang@wur.nl
MeSH Terms
- Animals
- Birds / genetics
- Birds / microbiology
- Birds / virology
- Body Size
- Borrelia burgdorferi / physiology
- Clutch Size
- Disease Reservoirs / microbiology
- Disease Reservoirs / veterinary
- Disease Reservoirs / virology
- Encephalitis Virus, Eastern Equine / physiology
- Encephalomyelitis, Eastern Equine / genetics
- Encephalomyelitis, Eastern Equine / virology
- Genetic Variation
- Horses / genetics
- Horses / microbiology
- Horses / virology
- Host Specificity
- Litter Size
- Lyme Disease / genetics
- Lyme Disease / microbiology
- Mammals / genetics
- Mammals / microbiology
- Mammals / virology
- Phylogeny
- Species Specificity
- West Nile Fever / genetics
- West Nile Fever / virology
- West Nile virus / physiology
Conflict of Interest Statement
The authors have declared that no competing interests exist.
References
This article includes 41 references
- Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. Global trends in emerging infectious diseases.. Nature 2008 Feb 21;451(7181):990-3.
- Cronin JP, Welsh ME, Dekkers MG, Abercrombie ST, Mitchell CE. Host physiological phenotype explains pathogen reservoir potential.. Ecol Lett 2010 Oct;13(10):1221-32.
- Kilpatrick AM, Daszak P, Jones MJ, Marra PP, Kramer LD. Host heterogeneity dominates West Nile virus transmission.. Proc Biol Sci 2006 Sep 22;273(1599):2327-33.
- Brunner JL, LoGiudice K, Ostfeld RS. Estimating reservoir competence of Borrelia burgdorferi hosts: prevalence and infectivity, sensitivity, and specificity.. J Med Entomol 2008 Jan;45(1):139-47.
- Komar N, Dohm DJ, Turell MJ, Spielman A. Eastern equine encephalitis virus in birds: relative competence of European starlings (Sturnus vulgaris).. Am J Trop Med Hyg 1999 Mar;60(3):387-91.
- Komar N, Langevin S, Hinten S, Nemeth N, Edwards E, Hettler D, Davis B, Bowen R, Bunning M. Experimental infection of North American birds with the New York 1999 strain of West Nile virus.. Emerg Infect Dis 2003 Mar;9(3):311-22.
- Johnson PT, Rohr JR, Hoverman JT, Kellermanns E, Bowerman J, Lunde KB. Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk.. Ecol Lett 2012 Mar;15(3):235-42.
- Miller MR, White A, Boots M. Host life span and the evolution of resistance characteristics.. Evolution 2007 Jan;61(1):2-14.
- Lee KA, Wikelski M, Robinson WD, Robinson TR, Klasing KC. Constitutive immune defences correlate with life-history variables in tropical birds.. J Anim Ecol 2008 Mar;77(2):356-63.
- Martin LB 2nd, Hasselquist D, Wikelski M. Investment in immune defense is linked to pace of life in house sparrows.. Oecologia 2006 Apr;147(4):565-75.
- Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS. Impacts of biodiversity on the emergence and transmission of infectious diseases.. Nature 2010 Dec 2;468(7324):647-52.
- Webster JP, Woolhouse MEJ. Cost of resistance: relationship between reduced fertility and increased resistance in a snail-schistosome host-parasite system.. P Roy Soc Lond B Bio 266: 391–396.
- LoGiudice K, Ostfeld RS, Schmidt KA, Keesing F. The ecology of infectious disease: effects of host diversity and community composition on Lyme disease risk.. Proc Natl Acad Sci U S A 2003 Jan 21;100(2):567-71.
- McKenzie NL, Burbidge AA, Baynes A, Brereton RN, Dickman CR. Analysis of factors implicated in the recent decline of Australia's mammal fauna.. J Biogeogr 34: 597–611.
- Cunningham AA, Dobson AP, Hudson PJ. Disease invasion: impacts on biodiversity and human health.. Philos Trans R Soc Lond B Biol Sci 2012 Oct 19;367(1604):2804-6.
- Gilbert GS, Webb CO. Phylogenetic signal in plant pathogen-host range.. Proc Natl Acad Sci U S A 2007 Mar 20;104(12):4979-83.
- Eisen L, Dolan MC, Piesman J, Lane RS. Vector competence of Ixodes pacificus and I. spinipalpis (Acari: Ixodidae), and reservoir competence of the dusky-footed woodrat (Neotoma fuscipes) and the deer mouse (Peromyscus maniculatus), for Borrelia bissettii.. J Med Entomol 2003 May;40(3):311-20.
- Kilpatrick AM, LaDeau SL, Marra PP. Ecology of west nile virus transmission and its impact on birds in the western hemisphere.. Auk 124: 1121–1136.
- Hackett SJ, Kimball RT, Reddy S, Bowie RC, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han KL, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T. A phylogenomic study of birds reveals their evolutionary history.. Science 2008 Jun 27;320(5884):1763-8.
- Felsenstein J. Phylogenies and the comparative method.. Am Nat 125: 1–15.
- Bininda-Emonds OR, Cardillo M, Jones KE, MacPhee RD, Beck RM, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A. The delayed rise of present-day mammals.. Nature 2007 Mar 29;446(7135):507-12.
- Martins EP, Hansen TF. Phylogenies and the comparative method: A general approach to incorporating phylogenetic information into the analysis of interspecific data.. Am Nat 149: 646–667.
- Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language.. Bioinformatics 2004 Jan 22;20(2):289-90.
- Lee KA. Linking immune defenses and life history at the levels of the individual and the species.. Integr Comp Biol 2006 Dec;46(6):1000-15.
- Rantala MJ, Roff DA. An analysis of trade-offs in immune function, body size and development time in the Mediterranean Field Cricket, Gryllus bimaculatus.. Funct Ecol 19: 323–330.
- Previtali MA, Ostfeld RS, Keesing F, Jolles AE, Hanselmann R. Relationship between pace of life and immune responses in wild rodents.. Oikos no–no.
- Cardillo M. Biological determinants of extinction risk: why are smaller species less vulnerable?. Animal Conservation 6: 63–69.
- Robinson JG, Redford KH. Body Size, Diet, and Population-Density of Neotropical Forest Mammals.. Am Nat 128: 665–680.
- Henle K, Davies KF, Kleyer M, Margules C, Settele J. Predictors of species sensitivity to fragmentation.. Biodivers Conserv 13: 207–251.
- Wood CL, Lafferty KD. Biodiversity and disease: a synthesis of ecological perspectives on Lyme disease transmission.. Trends Ecol Evol 2013 Apr;28(4):239-47.
- Roche B, Dobson AP, Guégan JF, Rohani P. Linking community and disease ecology: the impact of biodiversity on pathogen transmission.. Philos Trans R Soc Lond B Biol Sci 2012 Oct 19;367(1604):2807-13.
- Keesing F, Holt RD, Ostfeld RS. Effects of species diversity on disease risk.. Ecol Lett 2006 Apr;9(4):485-98.
- Allan BF, Keesing FS, Ostfeld RS. Effects of forest fragmentation on Lyme disease risk.. Conserv Biol 17: 267–272.
- Allan BF, Langerhans RB, Ryberg WA, Landesman WJ, Griffin NW, Katz RS, Oberle BJ, Schutzenhofer MR, Smyth KN, de St Maurice A, Clark L, Crooks KR, Hernandez DE, McLean RG, Ostfeld RS, Chase JM. Ecological correlates of risk and incidence of West Nile virus in the United States.. Oecologia 2009 Jan;158(4):699-708.
- Suzán G, Marcé E, Giermakowski JT, Mills JN, Ceballos G, Ostfeld RS, Armién B, Pascale JM, Yates TL. Experimental evidence for reduced rodent diversity causing increased hantavirus prevalence.. PLoS One 2009;4(5):e5461.
- Haas SE, Hooten MB, Rizzo DM, Meentemeyer RK. Forest species diversity reduces disease risk in a generalist plant pathogen invasion.. Ecol Lett 2011 Nov;14(11):1108-16.
- Johnson PT, Lund PJ, Hartson RB, Yoshino TP. Community diversity reduces Schistosoma mansoni transmission, host pathology and human infection risk.. Proc Biol Sci 2009 May 7;276(1662):1657-63.
- Searle CL, Biga LM, Spatafora JW, Blaustein AR. A dilution effect in the emerging amphibian pathogen Batrachochytrium dendrobatidis.. Proc Natl Acad Sci U S A 2011 Sep 27;108(39):16322-6.
- Clay CA, Lehmer EM, Jeor SS, Dearing MD. Sin nombre virus and rodent species diversity: a test of the dilution and amplification hypotheses.. PLoS One 2009 Jul 31;4(7):e6467.
- Swaddle JP, Calos SE. Increased avian diversity is associated with lower incidence of human West Nile infection: observation of the dilution effect.. PLoS One 2008 Jun 25;3(6):e2488.
- Randolph SE, Dobson AD. Pangloss revisited: a critique of the dilution effect and the biodiversity-buffers-disease paradigm.. Parasitology 2012 Jun;139(7):847-63.
Citations
This article has been cited 40 times.- Halliday FW, Czyżewski S, Laine AL. Intraspecific trait variation and changing life-history strategies explain host community disease risk along a temperature gradient.. Philos Trans R Soc Lond B Biol Sci 2023 Mar 27;378(1873):20220019.
- Nuismer SL, Basinski AJ, Schreiner C, Whitlock A, Remien CH. Reservoir population ecology, viral evolution and the risk of emerging infectious disease.. Proc Biol Sci 2022 Sep 14;289(1982):20221080.
- Mipam TD, Chen F, Tian L, Zhang P, Huang M, Chen L, Wang X, Zhang P, Lin Z, Liu X. Plant community-mediated effects of grazing on plant diseases.. Oecologia 2022 Aug;199(4):897-905.
- Estavillo C, Weyland F, Herrera L. Zoonotic Disease Risk and Life-History Traits: Are Reservoirs Fast Life Species?. Ecohealth 2022 Sep;19(3):390-401.
- Lin YP, Tufts DM, Combs M, Dupuis AP 2nd, Marcinkiewicz AL, Hirsbrunner AD, Diaz AJ, Stout JL, Blom AM, Strle K, Davis AD, Kramer LD, Kolokotronis SO, Diuk-Wasser MA. Cellular and immunological mechanisms influence host-adapted phenotypes in a vector-borne microparasite.. Proc Biol Sci 2022 Feb 23;289(1969):20212087.
- Humphreys JM, Pelzel-McCluskey AM, Cohnstaedt LW, McGregor BL, Hanley KA, Hudson AR, Young KI, Peck D, Rodriguez LL, Peters DPC. Integrating Spatiotemporal Epidemiology, Eco-Phylogenetics, and Distributional Ecology to Assess West Nile Disease Risk in Horses.. Viruses 2021 Sep 12;13(9).
- Seal S, Dharmarajan G, Khan I. Evolution of pathogen tolerance and emerging infections: A missing experimental paradigm.. Elife 2021 Sep 21;10.
- Keesing F, Ostfeld RS. Dilution effects in disease ecology.. Ecol Lett 2021 Nov;24(11):2490-2505.
- Wang YXG, Matson KD, Santini L, Visconti P, Hilbers JP, Huijbregts MAJ, Xu Y, Prins HHT, Allen T, Huang ZYX, de Boer WF. Mammal assemblage composition predicts global patterns in emerging infectious disease risk.. Glob Chang Biol 2021 Oct;27(20):4995-5007.
- Halliday FW, Jalo M, Laine AL. The effect of host community functional traits on plant disease risk varies along an elevational gradient.. Elife 2021 May 13;10.
- Keesing F, Ostfeld RS. Impacts of biodiversity and biodiversity loss on zoonotic diseases.. Proc Natl Acad Sci U S A 2021 Apr 27;118(17).
- Worsley-Tonks KEL, Escobar LE, Biek R, Castaneda-Guzman M, Craft ME, Streicker DG, White LA, Fountain-Jones NM. Using host traits to predict reservoir host species of rabies virus.. PLoS Negl Trop Dis 2020 Dec;14(12):e0008940.
- de Thoisy B, Silva NIO, Sacchetto L, de Souza Trindade G, Drumond BP. Spatial epidemiology of yellow fever: Identification of determinants of the 2016-2018 epidemics and at-risk areas in Brazil.. PLoS Negl Trop Dis 2020 Oct;14(10):e0008691.
- Halliday FW, Rohr JR, Laine AL. Biodiversity loss underlies the dilution effect of biodiversity.. Ecol Lett 2020 Nov;23(11):1611-1622.
- Stewart Merrill TE, Johnson PTJ. Towards a mechanistic understanding of competence: a missing link in diversity-disease research.. Parasitology 2020 Sep;147(11):1159-1170.
- Han BA, O'Regan SM, Paul Schmidt J, Drake JM. Integrating data mining and transmission theory in the ecology of infectious diseases.. Ecol Lett 2020 Aug;23(8):1178-1188.
- Vinson JE, Park AW. Vector-borne parasite invasion in communities across space and time.. Proc Biol Sci 2019 Dec 18;286(1917):20192614.
- Guth S, Visher E, Boots M, Brook CE. Host phylogenetic distance drives trends in virus virulence and transmissibility across the animal-human interface.. Philos Trans R Soc Lond B Biol Sci 2019 Sep 30;374(1782):20190296.
- Walsh MG. Ecological and life history traits are associated with Ross River virus infection among sylvatic mammals in Australia.. BMC Ecol 2019 Jan 15;19(1):2.
- Hofmeester TR, Krawczyk AI, van Leeuwen AD, Fonville M, Montizaan MGE, van den Berge K, Gouwy J, Ruyts SC, Verheyen K, Sprong H. Role of mustelids in the life-cycle of ixodid ticks and transmission cycles of four tick-borne pathogens.. Parasit Vectors 2018 Nov 20;11(1):600.
- Jansen AM, Xavier SCDC, Roque ALR. Trypanosoma cruzi transmission in the wild and its most important reservoir hosts in Brazil.. Parasit Vectors 2018 Sep 6;11(1):502.
- Guo F, Bonebrake TC, Gibson L. Land-Use Change Alters Host and Vector Communities and May Elevate Disease Risk.. Ecohealth 2019 Dec;16(4):647-658.
- Liu X, Chen F, Lyu S, Sun D, Zhou S. Random species loss underestimates dilution effects of host diversity on foliar fungal diseases under fertilization.. Ecol Evol 2018 Feb;8(3):1705-1713.
- Brace AJ, Lajeunesse MJ, Ardia DR, Hawley DM, Adelman JS, Buchanan KL, Fair JM, Grindstaff JL, Matson KD, Martin LB. Costs of immune responses are related to host body size and lifespan.. J Exp Zool A Ecol Integr Physiol 2017 Jun;327(5):254-261.
- Durand B, Tran A, Balança G, Chevalier V. Geographic variations of the bird-borne structural risk of West Nile virus circulation in Europe.. PLoS One 2017;12(10):e0185962.
- Plourde BT, Burgess TL, Eskew EA, Roth TM, Stephenson N, Foley JE. Are disease reservoirs special? Taxonomic and life history characteristics.. PLoS One 2017;12(7):e0180716.
- Kuno G, Mackenzie JS, Junglen S, Hubálek Z, Plyusnin A, Gubler DJ. Vertebrate Reservoirs of Arboviruses: Myth, Synonym of Amplifier, or Reality?. Viruses 2017 Jul 13;9(7).
- Faust CL, Dobson AP, Gottdenker N, Bloomfield LSP, McCallum HI, Gillespie TR, Diuk-Wasser M, Plowright RK. Null expectations for disease dynamics in shrinking habitat: dilution or amplification?. Philos Trans R Soc Lond B Biol Sci 2017 Jun 5;372(1722).
- Cable J, Barber I, Boag B, Ellison AR, Morgan ER, Murray K, Pascoe EL, Sait SM, Wilson AJ, Booth M. Global change, parasite transmission and disease control: lessons from ecology.. Philos Trans R Soc Lond B Biol Sci 2017 May 5;372(1719).
- Liu X, Lyu S, Sun D, Bradshaw CJ, Zhou S. Species decline under nitrogen fertilization increases community-level competence of fungal diseases.. Proc Biol Sci 2017 Jan 25;284(1847).
- Estrada-Peña A, Sprong H, Cabezas-Cruz A, de la Fuente J, Ramo A, Coipan EC. Nested coevolutionary networks shape the ecological relationships of ticks, hosts, and the Lyme disease bacteria of the Borrelia burgdorferi (s.l.) complex.. Parasit Vectors 2016 Sep 23;9(1):517.
- Araujo A, Kirschman L, Warne RW. Behavioural phenotypes predict disease susceptibility and infectiousness.. Biol Lett 2016 Aug;12(8).
- Johnson PT, Ostfeld RS, Keesing F. Frontiers in research on biodiversity and disease.. Ecol Lett 2015 Oct;18(10):1119-33.
- Hily JM, García A, Moreno A, Plaza M, Wilkinson MD, Fereres A, Fraile A, García-Arenal F. The relationship between host lifespan and pathogen reservoir potential: an analysis in the system Arabidopsis thaliana--cucumber mosaic virus.. PLoS Pathog 2014 Nov;10(11):e1004492.
- Ostfeld RS, Levi T, Jolles AE, Martin LB, Hosseini PR, Keesing F. Life history and demographic drivers of reservoir competence for three tick-borne zoonotic pathogens.. PLoS One 2014;9(9):e107387.
- Wojdak JM, Edman RM, Wyderko JA, Zemmer SA, Belden LK. Host density and competency determine the effects of host diversity on trematode parasite infection.. PLoS One 2014;9(8):e105059.
- Mihaljevic JR, Joseph MB, Orlofske SA, Paull SH. The scaling of host density with richness affects the direction, shape, and detectability of diversity-disease relationships.. PLoS One 2014;9(5):e97812.
- Chevalier V, Tran A, Durand B. Predictive modeling of West Nile virus transmission risk in the Mediterranean Basin: how far from landing?. Int J Environ Res Public Health 2013 Dec 20;11(1):67-90.
- Lacroix C, Jolles A, Seabloom EW, Power AG, Mitchell CE, Borer ET. Non-random biodiversity loss underlies predictable increases in viral disease prevalence.. J R Soc Interface 2014 Mar 6;11(92):20130947.
- Huang ZY, de Boer WF, van Langevelde F, Xu C, Ben Jebara K, Berlingieri F, Prins HH. Dilution effect in bovine tuberculosis: risk factors for regional disease occurrence in Africa.. Proc Biol Sci 2013 Aug 22;280(1765):20130624.
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