Climate change in the Arctic: testing the poleward expansion of ticks and tick-borne diseases

Abstract Climate change is most strongly felt in the polar regions of the world, with significant impacts for the species that live in these extreme environments. The arrival of parasites and pathogens from more temperate areas may become a significant problem for these populations, but current observations of parasite presence often lack a historical reference of prior absence. Observations in the high Arctic of the seabird tick Ixodes uriae suggested that this species recently expanded its range poleward. As this tick can have a direct impact on the breeding success of its seabird hosts and is vector of many potential disease agents, including Lyme disease spirochaetes, its presence and origin are important elements for predicting its impact on polar seabird populations. Here, we use population genetic data and host serology to test the hypothesis that Ixodes uriae has recently expanded into the Svalbard archipelago. Both Black-legged kittiwakes ( Rissa tridactyla ) and Thick-billed murres ( Uria lomvia ) were captured in Kongsfjorden, Spitsbergen and sampled for ticks and blood. Collected ticks were genotyped using microsatellite markers and population genetic analyses were carried out using data from 14 additional seabird colonies distributed across the tick’s northern distribution. In contrast to predictions based on a recent expansion, the Spitsbergen population showed high genetic diversity and significant differentiation from the more southern populations, suggesting long-term population isolation. Host serology also demonstrated a high exposure rate to Lyme disease spirochaetes (Bbsl). Targeted PCR on tick DNA extracts and sequencing identified the presence of Borrelia garinii in a Spitsbergen tick, confirming seabird exposure and demonstrating the presence of Lyme disease bacteria in the high Arctic for the first time. Taken together, results contradict the notion that Ixodes uriae has recently expanded into the high Arctic region. Rather, this tick has likely been present for some time, maintaining relatively high population sizes and an endemic transmission cycle of Bbsl spirochaetes. Close future observations of population infestation/infection rates will now be necessary to relate epidemiological changes to ongoing climate modifications. Author summary The climate in the Arctic is rapidly changing, and with it, the flora and fauna that live there. These new environmental conditions can favor the establishment of invasive species, including novel parasites and pathogens. Here, we use population genetic data and host serology to examine whether recent observations of ticks infesting breeding seabirds in the high Arctic represent a poleward expansion of the parasite. Contrary to predictions, tick populations showed no evidence of a recent colonization of the region. Ticks have likely be present for a relatively long time, maintaining high local diversity despite harsh environmental conditions and vectoring infectious agents among breeding birds. Indeed, we demonstrate the presence of Lyme disease spirochaetes in the high Arctic for the first time, with bacterial DNA found in one of the sampled ticks and seabird serology demonstrating high exposure to this pathogen. This Lyme disease agent has therefore likely been established in the region and circulating at low frequency between seabirds and ticks for some time.

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