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

Christopher P Kozakiewicz; Lauren Ricci; Austin H Patton; Amanda R Stahlke; Sarah A Hendricks; Mark J Margres; Manuel Ruiz-Aravena; David G Hamilton; Rodrigo Hamede; Hamish McCallum; Menna E Jones; Paul A Hohenlohe; Andrew Storfer

doi:10.1111/mec.15558

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

Mol Ecol. 2020 Sep;29(17):3217-3233. doi: 10.1111/mec.15558. Epub 2020 Aug 2.

Authors

Affiliations

¹ School of Biological Sciences, Washington State University, Pullman, WA, USA.
² Department of Integrative Biology, University of California, Berkeley, CA, USA.
³ Department of Biological Sciences, Institute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, ID, USA.
⁴ Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA.
⁵ School of Natural Sciences, University of Tasmania, Hobart, Tas., Australia.
⁶ Environmental Futures Research Institute, Griffith University, Nathan, Qld, Australia.

Abstract

Genetic structure in host species is often used to predict disease spread. However, host and pathogen genetic variation may be incongruent. Understanding landscape factors that have either concordant or divergent influence on host and pathogen genetic structure is crucial for wildlife disease management. Devil facial tumour disease (DFTD) was first observed in 1996 and has spread throughout almost the entire Tasmanian devil geographic range, causing dramatic population declines. Whereas DFTD is predominantly spread via biting among adults, devils typically disperse as juveniles, which experience low DFTD prevalence. Thus, we predicted little association between devil and tumour population structure and that environmental factors influencing gene flow differ between devils and tumours. We employed a comparative landscape genetics framework to test the influence of environmental factors on patterns of isolation by resistance (IBR) and isolation by environment (IBE) in devils and DFTD. Although we found evidence for broad-scale costructuring between devils and tumours, we found no relationship between host and tumour individual genetic distances. Further, the factors driving the spatial distribution of genetic variation differed for each. Devils exhibited a strong IBR pattern driven by major roads, with no evidence of IBE. By contrast, tumours showed little evidence for IBR and a weak IBE pattern with respect to elevation in one of two tumour clusters we identify herein. Our results warrant caution when inferring pathogen spread using host population genetic structure and suggest that reliance on environmental barriers to host connectivity may be ineffective for managing the spread of wildlife diseases. Our findings demonstrate the utility of comparative landscape genetics for identifying differential factors driving host dispersal and pathogen transmission.

Keywords: conservation genetics; disease biology; ecological genetics; host-parasite interactions; landscape genetics; population genetics-empirical.

Publication types

Research Support, N.I.H., Extramural
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Animals, Wild
Facial Neoplasms* / genetics
Facial Neoplasms* / veterinary
Genetic Structures
Marsupialia* / genetics

Grants and funding

R01 GM126563/GM/NIGMS NIH HHS/United States