Non-random biodiversity loss underlies predictable increases in viral disease prevalence Lacroix, C., Jolles, A., Seabloom, E. W., Power, A. G., Mitchell, C. E., & Borer, E. T. (2014). Non-random biodiversity loss underlies predictable increases in viral disease prevalence. Journal of the Royal Society Interface, 11(92) doi:10.1098/rsif.2013.0947 10.1098/rsif.2013.0947 The Royal Society Accepted Manuscript http://cdss.library.oregonstate.edu/sa-termsofuse Page 1 of 37 Under review for J. R. Soc. Interface 1 2 3 1 Non-random biodiversity loss underlies predictable increases in viral disease prevalence 4 5 6 2 7 8 3 Christelle Lacroix 1*, Anna Jolles 2,3 , Eric W. Seabloom 1, Alison G. Power 4, Charles E. Mitchell 5 9 10 4 1 11 and Elizabeth T. Borer 12 13 5 14 15 6 1 Department of Ecology, Evolution, and Behavior, University of Minnesota, Saint Paul, MN 16 17 18 7 55108, USA For Review Only 19 20 8 2 Department of Biomedical Sciences, Oregon State University, Corvallis, OR 97331, USA 21 22 9 3 Department of Zoology, Oregon State University, Corvallis, OR 9733, USA 23 24 4 25 10 Department of Ecology & Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA 26 27 11 5 Department of Biology, University of North Carolina, Chapel Hill, NC 27599 USA 28 29 12 *To whom correspondence should be addressed. Email: [email protected] 30 31 32 13 33 34 14 Abstract 35 36 37 15 38 39 40 16 Disease dilution (reduced disease prevalence with increasing biodiversity) has been described for 41 42 17 many different pathogens. Although the mechanisms causing this phenomenon remain unclear, 43 44 45 18 the disassembly of communities to predictable subsets of species, which can be caused by 46 47 19 changing climate, land use, or invasive species, underlie one important hypothesis. In this case, 48 49 50 20 infection prevalence will reflect the competence of the remaining hosts. To test this hypothesis, 51 52 21 we measured local host species abundance and prevalence of four generalist aphid-vectored 53 54 22 pathogens (barley and cereal yellow dwarf viruses) in a ubiquitous annual grass host at ten sites 55 56 57 23 spanning 2000 kilometers along the North American West Coast. In lab and field trials, we 58 59 60 1 http://mc.manuscriptcentral.com/jrsi Under review for J. R. Soc. Interface Page 2 of 37 1 2 3 24 measured viral infection, and aphid fecundity and feeding preference on several host species. 4 5 6 25 Virus prevalence increased as local host richness declined. Community disassembly was non- 7 8 26 random: ubiquitous hosts dominating species-poor assemblages were among the most competent 9 10 27 11 for vector production and virus transmission. This suggests that non-random biodiversity loss led 12 13 28 to increased virus prevalence. Because diversity loss is occurring globally in response to 14 15 29 anthropogenic changes, such work can inform medical, agricultural, and veterinary disease 16 17 18 30 research by providing Forinsights into Review the dynamics of pathogens Only nested within a complex web of 19 20 31 environmental forces. 21 22 23 24 32 25 26 33 Keywords 27 28 34 29 30 31 35 Barley and cereal yellow dwarf viruses (B/CYDVs, Luteoviridae), Bromus hordeaceus, 32 33 36 Rhopalosiphum padi (Aphididae), disease dilution, nestedness, vector-borne pathogen. 34 35 37 36 37 38 38 39 40 39 41 42 40 43 44 45 41 46 47 42 48 49 50 43 51 52 44 53 54 45 55 56 57 46 58 59 60 2 http://mc.manuscriptcentral.com/jrsi Page 3 of 37 Under review for J. R. Soc. Interface 1 2 3 47 1. Introduction 4 5 6 48 7 8 49 Traditionally, research on infectious diseases has taken place within isolated disciplines such as 9 10 50 11 plant pathology, human medicine, and veterinary medicine, and within these disciplines, research 12 13 51 labs and funding are often tied to specific hosts and pathogens [1]. However, many important 14 15 52 pathogens are host generalists and host-pathogen interactions can be governed by variable and 16 17 18 53 changing environmentalFor conditions Review such as temperature, rainfall,Only and nutrient supplies or the 19 20 54 presence of alternate hosts [2–5]. 21 22 55 23 24 25 56 Recent research in community and theoretical ecology has benefited from theoretical foundations 26 27 57 in statistical physics and mechanics and thus has provided important insights into the dynamics 28 29 58 of species distribution and interactions in complex systems [6–8]. In disease ecology, such 30 31 32 59 integrative work on host-pathogens interactions can be translated into better forecasting and 33 34 60 management of infectious disease [1] especially in the face of human alteration of the global 35 36 37 61 ecosystem. Importantly, altered abiotic regimes including global biogeochemical cycles and 38 39 62 biotic interactions including the spread of invasive species have led to global and local declines 40 41 63 in species diversity [9,10]. The simultaneous trends of accelerating loss of native biodiversity 42 43 44 64 [11,12] and emergence of infectious diseases [13–15] has spurred investigations into the role that 45 46 65 host species diversity can play in mediating host-parasite interactions [2,16,17]. Biodiversity can 47 48 66 modify infectious disease prevalence and risk through either an amplification or a dilution effect 49 50 51 67 [2]. Disease dilution, an important ecosystem service, has been reported for a variety of systems 52 53 68 from vector-borne zoonoses (i.e. diseases transmitted from animals to humans) to directly 54 55 69 transmitted plant pathogens [16,18–22]. However, a variety of mechanisms might underlie this 56 57 58 59 60 3 http://mc.manuscriptcentral.com/jrsi Under review for J. R. Soc. Interface Page 4 of 37 1 2 3 70 common pattern, and the effects of biodiversity on disease prevalence are still in debate [23–25]. 4 5 6 71 Examination of theoretical and empirical studies has revealed the importance of specific 7 8 72 characteristics of the hosts and parasites involved, of the type of metric used to assess disease 9 10 73 11 risk, of the spatial scale used to assess the biodiversity-disease relationship, and of changes in 12 13 74 host community structure versus diversity [23,26–28]. 14 15 75 16 17 18 76 When pathogen transmissionFor is density-dependent, Review as is typicalOnly for directly transmitted diseases 19 20 77 with a narrow host range and diseases transmitted by ‘sit-and-wait’ vectors (e.g. ticks), 21 22 78 biodiversity can alter infection prevalence through a change in the absolute abundance of hosts 23 24 25 79 and vectors [22,29–31]. The prevalence of generalist parasites with vectors that disperse over 26 27 80 long distances, thereby reducing the density-dependence of transmission, may also depend on 28 29 81 biodiversity under certain conditions [16,23,29,32] . In particular, reduced encounter probability 30 31 32 82 between susceptible hosts and infected vectors can reduce infection risk with increasing 33 34 83 biodiversity when host behavior or vector search efficiency is altered [2,33]. Disease prevalence 35 36 37 84 can also be affected by heterogeneity in competence of host reservoirs for parasite transmission 38 39 85 [32,34]. Taken together, this body of work points to the importance of host biodiversity for 40 41 86 controlling disease spread via interspecific variability in host competence and vector search 42 43 44 87 efficiency [2,26,32] . 45 46 88 47 48 89 The potential for hosts to affect the dynamics of generalist vector-borne parasites (host 49 50 51 90 competence) depends on several key epidemiological parameters including host susceptibility, 52 53 91 vector feeding preference and fecundity, and pathogen transmission, which can vary according to 54 55 92 host traits such as life history and physiological phenotype [35–37]. Thus, compositional shifts 56 57 58 59 60 4 http://mc.manuscriptcentral.com/jrsi Page 5 of 37 Under review for J. R. Soc. Interface 1 2 3 93 favouring highly competent species in communities are expected to increase transmission rate 4 5 6 94 leading to disease amplification [35,38], whereas an abundance of non- or poorly- competent 7 8 95 species would reduce disease incidence leading to dilution [23,32]. 9 10 96 11 12 13 97 The distinction between host diversity, host community composition, and trait variability [23] is 14 15 98 particularly important for predictions of disease prevalence with changing community 16 17 18 99 composition via reductionFor of species Review diversity. Realistic biodiverOnlysity losses have been shown to 19 20 100 disproportionally involve species characterized by particular sets of functional traits [39–41]. 21 22 101 Thus, depending on whether host species’ parameters that enhance pathogen spread co-vary with 23 24 25 102 the order of host species’ loss, the effects of biodiversity loss on disease prevalence could be 26 27 103 predicted by the order of species loss in community disassembly, and by traits of host species left 28 29 104 in communities [26]. The detection of a dilution effect for generalist vector-borne diseases would 30 31 32 105 thus require more competent hosts also to be more ubiquitous, i.e. to be present in species-poor 33 34 106 sites and to co-occur in species-rich communities with non- or poorly- competent species 35 36 37 107 [2,23,29,32] .