Pathogens in space: Advancing understanding of pathogen dynamics and disease ecology through landscape genetics

Abstract

Landscape genetics has provided many insights into how heterogeneous landscape features drive processes influencing spatial genetic variation in free‐living organisms. This rapidly developing field has focused heavily on vertebrates, and expansion of this scope to the study of infectious diseases holds great potential for landscape geneticists and disease ecologists alike. The potential application of landscape genetics to infectious agents has garnered attention at formative stages in the development of landscape genetics, but systematic examination is lacking. We comprehensively review how landscape genetics is being used to better understand pathogen dynamics. We characterize the field and evaluate the types of questions addressed, approaches used and systems studied. We also review the now established landscape genetic methods and their realized and potential applications to disease ecology. Lastly, we identify emerging frontiers in the landscape genetic study of infectious agents, including recent phylogeographic approaches and frameworks for studying complex multihost and host‐vector systems. Our review emphasizes the expanding utility of landscape genetic methods available for elucidating key pathogen dynamics (particularly transmission and spread) and also how landscape genetic studies of pathogens can provide insight into host population dynamics. Through this review, we convey how increasing awareness of the complementarity of landscape genetics and disease ecology among practitioners of each field promises to drive important cross‐disciplinary advances.

Comparative landscape genetics reveals differential effects of environment on host and pathogen genetic structure in Tasmanian devils (Sarcophilus harrisii) and their transmissible tumour

“…Further, there is often uncertainty as to whether observed contacts and movements reflect actual pathogen transmission and spread (Craft, 2015). In contrast, the spatial distribution of genetic variation contains signatures of past dispersal (in the case of the host) or spread (in the case of the pathogen) and often can be linked with environmental or ecological factors at fine spatial scales (Archie, Luikart, & Ezenwa, 2009;Biek & Real, 2010;Blanchong, Robinson, Samuel, & Foster, 2016;Hemming-Schroeder, Lo, Salazar, Puente, & Yan, 2018;Kozakiewicz et al, 2018). Knowledge of these relationships is critical to predicting the spread of wildlife diseases and can inform management strategies aimed at mitigating their impact.…”

“…Cote, Garant, Robert, Mainguy, & Pelletier, 2012;Talbot, Garant, Paquette, Mainguy, & Pelletier, 2012), and to improve the predictive power of models of disease spread (e.g. Davy, Martinez-Nunez, Willis, & Good, 2015;Kozakiewicz et al, 2018;Robinson et al, 2013;Wilder, Kunz, & Sorenson, 2015). However, pathogen genetic structure does not necessarily reflect that of the host, and pathogen transmission may be disconnected from patterns of host gene flow.…”

“…Cleary, Waits, & Finegan, 2017;Goldberg & Waits, 2010;Petren, Grant, Grant, & Keller, 2005;Trumbo, Spear, Baumsteiger, & Storfer, 2013;Zancolli, Rödel, Steffan-Dewenter, & Storfer, 2014). Even fewer multispecies studies have employed landscape genetics methods to study the dynamics of infectious diseases in wildlife systems (Biek & Real, 2010;Hemming-Schroeder et al, 2018;Kozakiewicz et al, 2018). Such comparative landscape genetics frameworks can provide valuable insights into how host-pathogen interactions shape patterns of disease transmission and spread across heterogeneous landscapes (Leo, Gonzalez, Millien, & Cristescu, 2016;Schwabl et al, 2017;Talbot et al, 2017).…”

Host relatedness and landscape connectivity shape pathogen spread in a large secretive carnivore

“…The extent to which pathogen spread reflects movement patterns of their hosts is enigmatic but important for controlling disease 1, 2 . If pathogen spread mirrors host gene flow, host genetic structure/differentiation could be a valuable proxy for pathogen spread and be used as a basis to inform disease control 3, 4 (e.g., male vampire bat [ Desmodus rotundus ] genetics closely mirrors phylogenetic structure of rabies 5 ). A close relationship between host gene flow and pathogen spread may also be evidence for increased transmission between related conspecifics, and could affect evolutionary pressures on the pathogen, as closely related hosts may be more likely to have similar imune environments 6 .…”

Suppression gene drive in continuous space can result in unstable persistence of both drive and wild-type alleles

“…Where evolution occurs over timescales that are short compared to the time it takes alleles to disperse across a population by migration, modeling based on the assumption of panmixia is often inadequate, and frameworks that explicitly incorporate spatial structure must be utilized to accurately predict evolutionary dynamics [1][2][3][4][5][6][7][8] .…”