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Evolution in Action - Climate Change, Biodiversity Dynamics and Emerging Infectious Disease
Evolution in Action - Climate Change, Biodiversity Dynamics and Emerging Infectious Disease
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
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Accelerating climate warming and environmental pertur- brought into close contact following breakdown in mechan- 2
bation constitute a critical threat to ecosystem integrity and isms for biogeographic and ecological isolation. Our current
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sustainability, the distribution and continuity of biodiversity, era differs from the Quaternary and earlier in that human
socio-economic stability, and changing interfaces and eco- activity accelerates the rate of introductions [18], so outbreaks
tones influencing patterns of disease [8,10–15]. The scope, may occur more frequently and over wider geographical
scale and pervasive nature of anthropogenic climate warming ranges. One reason, however, for a general belief that emer-
anticipate substantial impacts across the biosphere and necessi- ging diseases will be rare is the recognition that emerging
tate an integrative approach to understanding environmental diseases are often the result of pathogens switching hosts,
change that incorporates historical and contemporary insights and the conventional wisdom in evolutionary biology has
about the factors that have determined the structure and been that host switches are difficult to achieve [19]. One of
distribution of biodiverse systems. the most studied features of parasitism is pronounced conser-
During the past 10 000–15 000 years, agriculture, domesti- vatism (often termed specificity) in the range of hosts used
become generalists and generalists maintain the potential to pocket gophers is limited to the temperate zone, and the 3
become specialists. Otherwise, specialization becomes an group appears to have been restricted south of the Lauren-
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evolutionary ‘dead-end’. tide –Cordillera continental glaciers in North America
Episodic shifts in climate and environmental settings, in during sequential glacial maxima over the extent of the
conjunction with ecological mechanisms and host switching, Late Pliocene and Quaternary, with a primary radiation
are often critical determinants of parasite diversification being limited to a relatively brief temporal window between
[28,31–33], a view counter to more than a century of 4.2 and 1.8 Ma [43]. A burst of diversification for genera and
coevolutionary thinking about the structure and history species of pocket gophers, and presumably their louse para-
of host–parasite assemblages (for comprehensive reviews, sites, coincided with a substantial regime of episodic
see [23,24,34]). A new conceptual insight (termed the Stockholm variation in climate and habitat perturbation. Cyclical shifts
Paradigm because of the core principles emanating from four in climate have been identified as primary drivers for expan-
academic generations of researchers at Stockholm University; sion/contraction, isolation (often in restricted refugia) and
parasites of humans, livestock, crops (we include in this novel Arctic, the contemporary long range invasion of two proto- 4
pest phytophagous insects and parasitoids insects of ben- strongylids has occurred under contrasting mechanisms of
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eficial insects) and wildlife—will be common rather than recurrent migration (Varestrongylus in caribou) versus sporadic
rare events during episodes of climate change. This is because dispersal (U. pallikuukensis in muskoxen). Climate warming, in
host switching is initially driven by EF, and that is based on both cases, is a central driver in expanding distributions and
genetic capabilities already in the system. The paradigm successful establishment of the parasites on the island. Direct
assumes that there is a large space (Sloppy Fitness Space: insights into the dynamic processes linking climate, parasite
[26,27,50,51]) of potential hosts from which most pathogens developmental biology and host population ecology with the
are precluded by circumstances of time, space and origin. Cli- invasion and establishment of macroparasites are apparent.
mate change and the associated biotic expansion events make Distributions and central (core) ranges for host–parasite
much more of that space available, in which case switches are assemblages are determined by interactions defined by his-
expected to occur rapidly and often. Concurrently, biotic con- tory, biotic structure (interconnectivity within ecosystems
recurrent expansion into negative habitat, for example associated EF is small, host shifts are likely to be rare and attention 5
with migration, will not support establishment or introduction can be focused on managing each EID as it emerges. Little
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[58]; recurrent expansion and introduction may be negated in attention need be paid to its origins, beyond a search for
the short term by secondary development of non-permissive the taxonomic identity of the parasite acting as the pathogen,
environments. Although infection pressure in the sense of and its immediate reservoir. If the potential for EF is large,
geographical expansion may occur with migratory host popu- however, then host shifts are likely to be common, and a
lations (such as caribou or birds at high northern latitudes), more predictive, pre-emptive framework for managing EID
only a permissive environmental setting will result in introduc- will be needed, greatly increasing the challenge of an already
tion. A tipping point related to reductions in generation time, difficult problem.
population amplification and increasing infection pressure in Humanity has tended to react to emerging diseases as they
core range may be the antecedent for expansion under a positive occur, using our understanding of epidemiology in an attempt
shifting balance in peripheral habitats and environments. to mitigate the damage done. If the Stockholm Paradigm reflects
not limit the risk of EID. The planet is thus an evolutionary and insights exploring biodiversity and the effects of climate among 6
and ecological minefield of EID through which millions of lungworm faunas in Arctic ungulates.
Funding statement. Some aspects discussed herein represent contributions
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people, their crops and their livestock wander daily.
of the Beringian Coevolution Project and the Integrated Inventory of
Acknowledgements. D.R.B. and E.P.H. express thanks for critical discus- Biomes of the Arctic supported by the National Science Foundation
sion and conceptual development to C. Wiklund, S. Nylin, N. Janz (DEB-Biodiversity Discovery and Analysis-1258010–1256832–1256493)
(Stockholm University), S. J. Agosta (Virginia Commonwealth Uni- with funding to J. A. Cook (Museum of Southwestern Biology), E.P.H.,
versity) and W.A. Boeger (Universidad Federal do Paraná). E.P.H. K. E. Galbreath (Northern Michigan University), E. DeChaine (Western
thanks S. J. Kutz (University of Calgary) for 20 years of collaborations Washington University).
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