Projected effects of climate change on tick phenology and fitness of pathogens transmitted by the North American tick Ixodes scapularis

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Abstract

Ixodes scapularis is the principal tick vector of the Lyme borreliosis agent Borrelia burgdorferi and other tick-borne zoonoses in northeastern North America. The degree of seasonal synchrony of nymphal and larval ticks may be important in influencing the basic reproductive number of the pathogens transmitted by I. scapularis. Because the seasonal phenology of tick vectors is partly controlled by ambient temperature, climate and climate change could shape the population biology of tick-borne pathogens. We used projected monthly normal temperatures, obtained from the second version of the Canadian Coupled Global Climate Model (CGCM2) under emissions scenario A2 of the Intergovernmental Panel on Climate Change for a site in southern Ontario, Canada, to simulate the phenology of I. scapularis in a mathematical model. The simulated seasonal abundance of ticks then determined transmission of three candidate pathogens amongst a population of white-footed mice (Peromyscus leucopus) using a susceptible–infected–recovered (SIR) model. Fitness of the different pathogens, in terms of resilience to changes in tick and rodent mortality, minima for infection duration, transmission efficiency and particularly any additional mortality of rodents specifically associated with infection, varied according to the seasonal pattern of immature tick activity, which was different under the temperature conditions projected for the 2020s, 2050s and 2080s. In each case, pathogens that were long-lived, highly transmissible and had little impact on rodent mortality rates were the fittest. However, under the seasonal tick activity patterns projected for the 2020s and 2050s, the fitness of pathogens that are shorter-lived, less efficiently transmitted, and more pathogenic to their natural hosts, increased. Therefore, climate change may affect the frequency and distribution of I. scapularis-borne pathogens and alter their evolutionary trajectories.

Introduction

Ixodes scapularis is the tick vector of a number of zoonoses, including Lyme borreliosis, the most frequent vector-borne disease of humans in the temperate zone (Kurtenbach et al., 2006). Climate change is anticipated to have an impact on the global risk from arthropod-borne diseases in two ways. First, a warming climate is anticipated to drive changes in the geographic ranges of arthropod disease vectors (including the ticks I. scapularis and I. ricinus in North America and Europe, respectively: Lindgren et al., 2000; Ogden et al., 2006). Second, changes of the geographic ranges of vector-borne pathogens are likely to follow suit, but the existence of endemic transmission cycles of vector-borne pathogens (i.e. where the basic reproductive number, R0, of the pathogen is greater than one) may depend on more stringent criteria than just presence or absence of vectors, and these may also be affected by climate (Rogers and Randolph, 2006).

The rate of pathogen transmission by ixodid (hard-bodied) ticks such as I. scapularis, which feed only once per active life stage, is determined by the time it takes for an engorged tick that fed on an infected host to develop and moult into the next life stage (e.g. larva to nymph, or nymph to adult female: Randolph, 1998). Interstadial development is temperature-dependent, of protracted duration (frequently several months) and, because it takes place off the vertebrate host in the superficial layers of the soil and the litter layer, it is influenced by ambient climate (Lindsay et al., 1999; Ogden et al., 2004). For most pathogens transmitted by I. scapularis and I. ricinus, transmission cycles involve (i) infected nymphs feeding on susceptible hosts (rodents or other terrestrial vertebrates), (ii) transmission of the pathogens from these hosts to uninfected larvae, and (iii) engorgement and development, and moulting of larvae into infective nymphs to complete the cycle (Thompson et al., 2001).

For transmission cycles of tick-borne pathogens to persist, in the absence of efficient transovarial transmission from engorged adult female to larval ticks, larvae and nymphs must feed on the same hosts within a time period that spans the duration of infectiousness of the host. The degree of synchrony of the seasonal appearance of active, infective nymphal and uninfected larval ticks can be a crucial factor determining R0 of pathogens transmitted by ixodid ticks (Randolph et al., 2000). The seasonal synchrony of different instars is a function of the phenology of the whole tick lifecycle, which, being determined by temperature-dependent development rates, climate-dependent tick activity, as well as temperature-independent diapause, is potentially affected by climate change (Randolph, 2001; Ogden et al., 2006).

A mechanistic model of I. scapularis populations, built to understand how climate could affect seasonality and survival of I. scapularis (Ogden et al., 2005), suggested that ambient temperature is a significant driver of the different patterns of I. scapularis seasonality seen at different latitudes in North America (Ogden et al., 2006). Consequently, we have raised the hypothesis that by affecting the degree of seasonal synchrony of different tick instars, climate may be an important determinant of fitness of tick-borne pathogens, and thus important in their evolutionary biology and emergence (Kurtenbach et al., 2006). We have developed a susceptible–infected–recovered (SIR) model for I. scapularis-borne pathogens, in which transmission rates amongst white-footed mice (Peromyscus leucopus) reservoirs were governed by the I. scapularis model (Ogden et al., 2007). In this model, simulated asynchronous seasonal activity of immature I. scapularis seen in northeastern North America (Wilson and Spielman, 1985) was a strong fitness determinant driving the evolution of pathogen traits that, in their natural hosts, permit infections that are persistent, highly transmissible to ticks and of low pathogenicity (Ogden et al., 2007). Here we model more explicitly the potential effects of climate change on the fitness of different I. scapularis-borne pathogens via changes in the degree of seasonal asynchrony of I. scapularis.

Section snippets

Model structure

The model, described in detail in Ogden et al. (2007), comprises two components: (i) a simulation model of I. scapularis (Ogden et al., 2005) to provide values for the daily number of infected and uninfected ticks attaching to, and detaching from, hosts in a seasonal cycle representative of conditions in northeastern North America, and (ii) an SIR or SIC (susceptible–infected–carrier: Kurtenbach et al., 2006) model of a host for larval and nymphal I. scapularis and tick-borne microparasites,

Simulated seasonality

The seasonality of I. scapularis in simulations for each temperature regime is presented in Fig. 2. The observed variation in seasonality was due to changes in two areas of the tick life-cycle. First, the pre-oviposition period for engorged females, and the pre-eclosion (egg development) period, become shorter with increasing spring and summer temperature (Ogden et al., 2004, Ogden et al., 2005), so larvae emerge and are active earlier in the year. Simulated larval activity peaked in the first

Discussion

In this study we investigated in detail how projected climate change could influence the seasonality of I. scapularis at the northern margin of the range of this tick. We then investigated to what extent the projected changes in immature tick seasonality could affect the fitness and survival of pathogens transmitted by this tick. While our model aims to capture and use real values for some key parameters when simulating transmission under current temperature conditions, our conclusions on

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