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Increased Diversity of Zoonotic Pathogens and Borrelia Burgdorferi Infection, Genetics and Evolution 27 (2014) 531–542 Contents lists available at ScienceDirect Infection, Genetics and Evolution journal homepage: www.elsevier.com/locate/meegid Increased diversity of zoonotic pathogens and Borrelia burgdorferi strains in established versus incipient Ixodes scapularis populations across the Midwestern United States ⇑ Sarah A. Hamer a, , Graham J. Hickling b, Edward D. Walker c, Jean I. Tsao c a Texas A&M University, 4458 TAMU, College Station, TX 77843, USA b University of Tennessee, 274 Ellington Plant Science Building, Knoxville, TN 37996, USA c Michigan State University, 13 Natural Resources Building, East Lansing, MI 48823, USA article info abstract Article history: The center of origin theory predicts that genetic diversity will be greatest near a specie’s geographic ori- Received 16 January 2014 gin because of the length of time for evolution. By corollary, diversity will decrease with distance from Received in revised form 2 June 2014 the origin; furthermore, invasion and colonization are frequently associated with founder effects that Accepted 6 June 2014 reduce genetic variation in incipient populations. The blacklegged tick, Ixodes scapularis, harbors a suite Available online 18 June 2014 of zoonotic pathogens, and the geographic range of the tick is expanding in the upper Midwestern United States. Therefore, we posited that diversity of I. scapularis-borne pathogens across its Midwestern range Keywords: should correlate with the rate of the range expansion of this tick as well as subsequent disease emer- Ixodes scapularis gence. Analysis of 1565 adult I. scapularis ticks from 13 sites across five Midwestern states revealed that Borrelia burgdorferi Anaplasma tick infection prevalence with multiple microbial agents (Borrelia burgdorferi, Borrelia miyamotoi, Babesia Babesia odocoilei, Babesia microti, and Anaplasma phagocytophilum), coinfections, and molecular genetic diversity American Midwest of B. burgdorferi all were positively correlated with the duration of establishment of tick populations, and therefore generally support the center of origin – pathogen diversity hypothesis. The observed differences across the gradient of establishment, however, were not strong and were nuanced by the high frequency of coinfections in tick populations at both established and recently-invaded tick populations. These results suggest that the invasion of ticks and their associated pathogens likely involve multiple means of pathogen introduction, rather than the conventionally presented scenario whereby infected, invading ticks are solely responsible for introducing pathogens to naïve host populations. Ó 2014 Elsevier B.V. All rights reserved. 1. Introduction borne pathogens and the diseases they cause are inextricably linked to that of their invertebrate vectors (Gubler, 1998; Otranto In biogeographical studies, a center of origin is a geographical et al., 2009), the patterns of invasion and establishment of vectors area where a group of organisms first developed its distinctive can often be used to predict disease risk. Similarly, pathogen diver- properties (Cain, 1943). This concept is typically applied to studies sity and prevalence may provide an indirect understanding of the of crop domestication and is a foundational principle of dispersal history of the disease system, as well as of the underlying ecolog- biogeography (Crisci et al., 2003). One may predict that the center ical and evolutionary processes. of genetic diversity of a pathogen is also at its center of origin due Ixodes scapularis, the blacklegged tick, is an epidemiologically to the length of time available for evolution (Wang et al., 1999a). important vector of multiple zoonotic pathogens in the upper Mid- Diversity is predicted to decrease with distance from the origin, western and Northeastern United States. Spielman (1988) hypoth- because invasion and colonization events are associated with foun- esized that historically, blacklegged ticks likely were widespread der effects that reduce genetic variation in incipient populations throughout eastern North America prior to the Pleistocene glacia- (Carlson and Templeton, 1984), and less time has been available tion, but then were restricted to refugia in the northeastern United for local drift and adaptation. Because the distribution of vector- States and northwestern Wisconsin. After the glaciers receded 10,000 years ago, relict populations putatively remained (Spielman, 1988). In the mid-twentieth century, the reversion of ⇑ Corresponding author. Tel.: +1 979 847 5693. agricultural lands to forest and implementation of hunting regula- E-mail addresses: [email protected] (S.A. Hamer), [email protected] (G.J. Hickling), [email protected] (E.D. Walker), [email protected] (J.I. Tsao). tions that allowed deer populations to increase in number http://dx.doi.org/10.1016/j.meegid.2014.06.003 1567-1348/Ó 2014 Elsevier B.V. All rights reserved. 532 S.A. Hamer et al. / Infection, Genetics and Evolution 27 (2014) 531–542 supported expansion of I. scapularis and its vertebrate hosts from 2. Materials and methods these refugia (Matuschka and Spielman, 1986). I. scapularis contin- ues to spread from endemic areas both in the Northeastern and 2.1. Field sites and tick samples Midwestern United States, but the mechanisms for this spread are not established. Across the Midwest, a gradient of establish- Ticks were sampled by drag cloth during the spring adult I. scap- ment of I. scapularis is apparent (Table 1), with tick populations ularis questing season (15 April–15 May) of 2006–2007 at 13 sites first detected in Wisconsin (WI), Minnesota (MN), Michigan’s across the Midwest (Fig. 1, Table 1): Castle Rock State Park, Ogle (MI) Upper Peninsula, and northwestern Illinois (IL) (Bouseman Co., IL; Indiana Dunes National Lakeshore, Porter Co., IN; Tippeca- et al., 1990; Drew et al., 1988; Jackson and Defoliart, 1970; noe River State Park, Pulaski Co., IN; Van Buren State Park, Van Strand et al., 1992), later detected in northern Indiana (IN) Buren Co., MI; Duck Lake State Park, Muskegon Co., MI; Fort McCoy (Bouseman et al., 1990; Cortinas and Kitron, 2006; Pinger and Military Instillation, Monroe Co., WI; Governor Dodge State Park, Glancy, 1989; Pinger et al., 1991, 1996), and most recently Iowa Co., WI; Saugatuck Dunes State Park, Allegan Co., MI; Menom- detected in the Chicago-area of Illinois (Jobe et al., 2006, 2007; inee North and South, Menominee Co., MI; Churchill Woods Forest Rydzewski et al., 2012) and Michigan’s Lower Peninsula (Foster, Preserve, DuPage Co., IL; Fort Sheridan, Lake Co., IL; and St. Croix 2004; Hamer et al., 2007, 2010). State Forest, Pine Co., MN. We targeted the spring peak of activity Currently, the three most epidemiologically significant I. scapu- of the adult life stage because adults have had two prior blood laris-borne zoonotic pathogens are Borrelia burgdorferi, Anaplasma meals and therefore have had a greater chance of being infected phagocytophilum, and Babesia microti. All three pathogens have in comparison to nymphs. Within each park, drag sampling was similar life histories, in which wild rodents serve as important res- restricted to the forest floor of closed-canopy, deciduous forest ervoirs (Donahue et al., 1987; Levin et al., 2002; Stancil, 1999; habitat, as this habitat type was positively correlated with I. scap- Telford and Spielman, 1993; Walls et al., 1997) and disease results ularis presence in a Midwestern habitat suitability model (Guerra when I. scapularis infected by wildlife serves as a bridge vector to et al., 2002), and a previous national tick survey also applied this humans. Several other pathogens have been recently detected in sampling criterion (Diuk-Wasser et al., 2006). Due to close geo- I. scapularis, including the relapsing fever spirochete B. miyamotoi. graphic proximity (between 30 and 70 km between sites), similar This pathogen was originally described in Ixodes persulcatus ticks in tick establishment timing, similar drag densities, and low individ- Japan (Fukunaga et al., 1995), and was recently determined to ual sample sizes, we grouped the two Chicago area sites (Chicago cause human disease in Russia and the US (Gugliotta et al., 2013; North and South), the two Michigan Upper Peninsula sites Krause et al., 2013; Platonov et al., 2011). (Menominee North and South), and two Michigan Lower Peninsula We tested the center of origin theory using I. scapularis and associ- sites (Saugatuck and Duck Lake) for our analyses. Based on the ated pathogens not only to apply this theory to a vector-borne disease approximate times when I. scapularis populations were first docu- system for the first time, but also to learn more about the invasion mented at these sites, we assigned them to three groups based on biology of these organisms. Given the close association of I. scapularis history of establishment of tick populations, as follows: Minnesota, and the pathogens it transmits, we posited that patterns of prevalence Wisconsin, western Illinois, and Michigan Upper Peninsula sites and diversity of I. scapularis-borne pathogens across its Midwestern are ‘long-established;’ northern Indiana sites are ‘intermediate- range may reflect the order of invasion and may be useful in better established;’ and Chicago-area and lower Michigan sites are understanding the mechanisms underlying the broad-scale invasion ‘recently-invaded’. Importantly, these establishment designations of this tick and subsequent disease emergence. Herein we hypothe- were assigned not only
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