Evolution in action: Climate change, biodiversity dynamics and emerging infectious disease

Authors: Hoberg, Eric; BROOKS, DANIEL - University Of Nebraska

Submitted to: Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/18/2014
Publication Date: 2/15/2015
Citation: Hoberg, E.P., Brooks, D.R. 2015. Evolution in action: Climate change, biodiversity dynamics and emerging infectious disease. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 370:1665. DOI: 10.1098/rstb.2013.0553.

Interpretive Summary: Understanding the dynamics of emerging infectious disease and vector-borne disease agents and the role of environmental and climatological influences in origins and dissemination is to a large extent based on our perceptions about the processes that govern complex interactions among host and pathogen species. We explore the contrasts apparent between the prevalent concepts of narrow coevolution (associations linked by evolutionary descent) and a substantially more nuanced and complex picture of how the biosphere has developed in both evolutionary (deep) and ecological (contemporary) time. We explore an emerging view for considerable complexity in the biosphere and world around us, and examine the implications for an increasingly robust understanding of mechanisms that determine the distribution of disease agents among hosts and across geographic regions. We demonstrate that climatological variation and ecological disturbance have been pervasive drivers of faunal assembly, structure and diversification for parasites and pathogens through recurrent events of geographic and host colonization at varying spatial and temporal scales of Earth history. Episodic shifts in climate and environmental settings, in conjunction with ecological mechanisms and host switching, are often critical determinants of parasite diversification, a view counter to more than a century of coevolutionary thinking about the nature of complex host-parasite assemblages. Processes now unfolding through contemporary and accelerating climate warming are having a substantial influence on the occurrence of parasites and the potential for emergent disease. The current crisis for emerging infectious disease (EID) is “new” only in the sense that this is the first such event that scientists have witnessed directly. Previous episodes through earth history of global climate change and ecological perturbation, broadly defined, have been associated with environmental disruptions that led to EID. From an epidemiological standpoint, episodes of global climate change should be expected to be associated with the origins of new host-parasite associations and bursts of EID. Our view provides a pathway to shift from a mode of reaction (to EID) toward one based on a proactive stance that emphasizes our developing knowledge base for the history and distribution of diversity and how we can use insights from history to anticipate unfolding changes in the structure of biological systems. Implications are abundant with respect to addressing emergent disease for people, our food resources, and among wildlife species. Conceptually our explorations are of importance to disease ecologists, parasitologists, and conservation biologists globally, and to an assemblage of scientists populating federal and state agencies across North America.

Technical Abstract: Climatological variation and ecological perturbation have been pervasive drivers of faunal assembly, structure and diversification for parasites and pathogens through recurrent events of geographic and host colonization at varying spatial and temporal scales of Earth history. Episodic shifts in climate and environmental settings, in conjunction with ecological mechanisms and host switching, are often critical determinants of parasite diversification, a view counter to more than a century of coevolutionary thinking about the nature of complex host-parasite assemblages. Parasites are resource specialists with restricted host ranges, yet shifts onto relatively unrelated hosts are common during phylogenetic diversification of parasite lineages and directly observable in real time. The emerging Stockholm Paradigm resolves this paradox: Ecological Fitting - phenotypic flexibility and phylogenetic conservatism in traits related to resource use, most notably host preference - provides many opportunities for rapid host switching in changing environments, without the evolution of novel host-utilization capabilities. Host shifts via ecological fitting fuel the expansion phase of the Oscillation Hypothesis of host range and speciation and, more generally, the generation of novel combinations of interacting species within the Geographic Mosaic Theory of Coevolution. In synergy, an environmental dynamic of Taxon Pulses establishes an episodic context for host and geographic colonization.