Landscape genetics of the Tasmanian devil: implications for spread of an infectious cancer

Andrew Storfer, Brendan Epstein, Menna Jones, Steven Micheletti, Stephen F. Spear, Shelly Lachish, Samantha Fox

Research output: Contribution to journalArticle

6 Citations (Scopus)

Abstract

Emerging infectious diseases are increasingly recognized in species’ declines and extinctions. Landscape genetics can be used as a tool to predict disease emergence and spread. The Tasmanian devil is threatened with extinction by a nearly 100% fatal transmissible cancer, which has spread across 95% of the species’ geographic range in 20 years. Here, we present a landscape genetic analysis in the last remaining uninfected parts of the Tasmanian devil’s geographic range to: describe population genetic structure, characterize genetic diversity, and test the influence of landscape variables on Tasmanian devil gene flow to assess the potential for disease spread. In contrast to previous genetic studies on Tasmanian devils showing evidence for two genetic populations island-wide, our genetic based assignment tests and spatial principal components analyses suggest at least two, and possibly three, populations in a study area that is approximately 15% of the size of the overall species’ geographic range. Positive spatial autocorrelation declined at about 40 km, in contrast to 80 km in eastern populations, highlighting the need for range-wide genetic studies. Strong genetic structure was found between devils in the northern part of the study area and those found south of Macquarie Harbor, with weaker structure found between the northeastern and northwestern portion of our study area. Consistent with previous work, we found low overall genetic diversity, likely owing to a combination of founder effects and extreme weather events thousands of years ago that likely caused large-scale population declines. We also found possible signs of recent bottlenecks, perhaps resulting from forest clearing for dairy farming in the central part of the study area. This human disturbance also may have contributed to weak genetic structuring detected between the northeastern and northwestern part of the study area. Individual-based least cost path modeling showed limited influence of landscape variables on gene flow, with weak effects of variation in elevation in the northeast. In the northwest, however, landscape genetic models did not perform better than the null isolation-by-distance model. At the larger spatial scale of the northern part of the study area, elevation and temperatures were negatively correlated with gene flow, consistent with low dispersal suitability of higher elevation habitats that have lower temperatures and dense, wet vegetation. Overall, Tasmanian devils are a highly vagile species for which dispersal and gene flow appear to be influenced little by landscape features, and spread of devil facial tumor disease to the remaining portion of the devil’s geographic range seems imminent. Nonetheless, strong genetic structure found between the northern and southern portions of our study area, combined with low densities and limited possible colonization of DFTD from the east suggest there is some time for implementation of management strategies.

Original languageEnglish (US)
Pages (from-to)1287-1297
Number of pages11
JournalConservation Genetics
Volume18
Issue number6
DOIs
StatePublished - Dec 1 2017

Fingerprint

Gene Flow
Genetic Structures
cancer
neoplasms
gene flow
Population Genetics
genetic structure
Neoplasms
Biological Extinction
Emerging Communicable Diseases
Population
Founder Effect
Time Management
population genetics
Spatial Analysis
Temperature
Genetic Models
Weather
Principal Component Analysis
Agriculture

Keywords

  • Devil facial tumor disease
  • Emerging infectious diseases
  • Landscape genetics
  • Tasmanian devil

Cite this

Landscape genetics of the Tasmanian devil : implications for spread of an infectious cancer. / Storfer, Andrew; Epstein, Brendan; Jones, Menna; Micheletti, Steven; Spear, Stephen F.; Lachish, Shelly; Fox, Samantha.

In: Conservation Genetics, Vol. 18, No. 6, 01.12.2017, p. 1287-1297.

Research output: Contribution to journalArticle

Storfer, A, Epstein, B, Jones, M, Micheletti, S, Spear, SF, Lachish, S & Fox, S 2017, 'Landscape genetics of the Tasmanian devil: implications for spread of an infectious cancer', Conservation Genetics, vol. 18, no. 6, pp. 1287-1297. https://doi.org/10.1007/s10592-017-0980-4
Storfer, Andrew ; Epstein, Brendan ; Jones, Menna ; Micheletti, Steven ; Spear, Stephen F. ; Lachish, Shelly ; Fox, Samantha. / Landscape genetics of the Tasmanian devil : implications for spread of an infectious cancer. In: Conservation Genetics. 2017 ; Vol. 18, No. 6. pp. 1287-1297.
@article{05e9aee07c1c4fff8d6250c5f590bc96,
title = "Landscape genetics of the Tasmanian devil: implications for spread of an infectious cancer",
abstract = "Emerging infectious diseases are increasingly recognized in species’ declines and extinctions. Landscape genetics can be used as a tool to predict disease emergence and spread. The Tasmanian devil is threatened with extinction by a nearly 100{\%} fatal transmissible cancer, which has spread across 95{\%} of the species’ geographic range in 20 years. Here, we present a landscape genetic analysis in the last remaining uninfected parts of the Tasmanian devil’s geographic range to: describe population genetic structure, characterize genetic diversity, and test the influence of landscape variables on Tasmanian devil gene flow to assess the potential for disease spread. In contrast to previous genetic studies on Tasmanian devils showing evidence for two genetic populations island-wide, our genetic based assignment tests and spatial principal components analyses suggest at least two, and possibly three, populations in a study area that is approximately 15{\%} of the size of the overall species’ geographic range. Positive spatial autocorrelation declined at about 40 km, in contrast to 80 km in eastern populations, highlighting the need for range-wide genetic studies. Strong genetic structure was found between devils in the northern part of the study area and those found south of Macquarie Harbor, with weaker structure found between the northeastern and northwestern portion of our study area. Consistent with previous work, we found low overall genetic diversity, likely owing to a combination of founder effects and extreme weather events thousands of years ago that likely caused large-scale population declines. We also found possible signs of recent bottlenecks, perhaps resulting from forest clearing for dairy farming in the central part of the study area. This human disturbance also may have contributed to weak genetic structuring detected between the northeastern and northwestern part of the study area. Individual-based least cost path modeling showed limited influence of landscape variables on gene flow, with weak effects of variation in elevation in the northeast. In the northwest, however, landscape genetic models did not perform better than the null isolation-by-distance model. At the larger spatial scale of the northern part of the study area, elevation and temperatures were negatively correlated with gene flow, consistent with low dispersal suitability of higher elevation habitats that have lower temperatures and dense, wet vegetation. Overall, Tasmanian devils are a highly vagile species for which dispersal and gene flow appear to be influenced little by landscape features, and spread of devil facial tumor disease to the remaining portion of the devil’s geographic range seems imminent. Nonetheless, strong genetic structure found between the northern and southern portions of our study area, combined with low densities and limited possible colonization of DFTD from the east suggest there is some time for implementation of management strategies.",
keywords = "Devil facial tumor disease, Emerging infectious diseases, Landscape genetics, Tasmanian devil",
author = "Andrew Storfer and Brendan Epstein and Menna Jones and Steven Micheletti and Spear, {Stephen F.} and Shelly Lachish and Samantha Fox",
year = "2017",
month = "12",
day = "1",
doi = "10.1007/s10592-017-0980-4",
language = "English (US)",
volume = "18",
pages = "1287--1297",
journal = "Conservation Genetics",
issn = "1566-0621",
publisher = "Springer Netherlands",
number = "6",

}

TY - JOUR

T1 - Landscape genetics of the Tasmanian devil

T2 - implications for spread of an infectious cancer

AU - Storfer, Andrew

AU - Epstein, Brendan

AU - Jones, Menna

AU - Micheletti, Steven

AU - Spear, Stephen F.

AU - Lachish, Shelly

AU - Fox, Samantha

PY - 2017/12/1

Y1 - 2017/12/1

N2 - Emerging infectious diseases are increasingly recognized in species’ declines and extinctions. Landscape genetics can be used as a tool to predict disease emergence and spread. The Tasmanian devil is threatened with extinction by a nearly 100% fatal transmissible cancer, which has spread across 95% of the species’ geographic range in 20 years. Here, we present a landscape genetic analysis in the last remaining uninfected parts of the Tasmanian devil’s geographic range to: describe population genetic structure, characterize genetic diversity, and test the influence of landscape variables on Tasmanian devil gene flow to assess the potential for disease spread. In contrast to previous genetic studies on Tasmanian devils showing evidence for two genetic populations island-wide, our genetic based assignment tests and spatial principal components analyses suggest at least two, and possibly three, populations in a study area that is approximately 15% of the size of the overall species’ geographic range. Positive spatial autocorrelation declined at about 40 km, in contrast to 80 km in eastern populations, highlighting the need for range-wide genetic studies. Strong genetic structure was found between devils in the northern part of the study area and those found south of Macquarie Harbor, with weaker structure found between the northeastern and northwestern portion of our study area. Consistent with previous work, we found low overall genetic diversity, likely owing to a combination of founder effects and extreme weather events thousands of years ago that likely caused large-scale population declines. We also found possible signs of recent bottlenecks, perhaps resulting from forest clearing for dairy farming in the central part of the study area. This human disturbance also may have contributed to weak genetic structuring detected between the northeastern and northwestern part of the study area. Individual-based least cost path modeling showed limited influence of landscape variables on gene flow, with weak effects of variation in elevation in the northeast. In the northwest, however, landscape genetic models did not perform better than the null isolation-by-distance model. At the larger spatial scale of the northern part of the study area, elevation and temperatures were negatively correlated with gene flow, consistent with low dispersal suitability of higher elevation habitats that have lower temperatures and dense, wet vegetation. Overall, Tasmanian devils are a highly vagile species for which dispersal and gene flow appear to be influenced little by landscape features, and spread of devil facial tumor disease to the remaining portion of the devil’s geographic range seems imminent. Nonetheless, strong genetic structure found between the northern and southern portions of our study area, combined with low densities and limited possible colonization of DFTD from the east suggest there is some time for implementation of management strategies.

AB - Emerging infectious diseases are increasingly recognized in species’ declines and extinctions. Landscape genetics can be used as a tool to predict disease emergence and spread. The Tasmanian devil is threatened with extinction by a nearly 100% fatal transmissible cancer, which has spread across 95% of the species’ geographic range in 20 years. Here, we present a landscape genetic analysis in the last remaining uninfected parts of the Tasmanian devil’s geographic range to: describe population genetic structure, characterize genetic diversity, and test the influence of landscape variables on Tasmanian devil gene flow to assess the potential for disease spread. In contrast to previous genetic studies on Tasmanian devils showing evidence for two genetic populations island-wide, our genetic based assignment tests and spatial principal components analyses suggest at least two, and possibly three, populations in a study area that is approximately 15% of the size of the overall species’ geographic range. Positive spatial autocorrelation declined at about 40 km, in contrast to 80 km in eastern populations, highlighting the need for range-wide genetic studies. Strong genetic structure was found between devils in the northern part of the study area and those found south of Macquarie Harbor, with weaker structure found between the northeastern and northwestern portion of our study area. Consistent with previous work, we found low overall genetic diversity, likely owing to a combination of founder effects and extreme weather events thousands of years ago that likely caused large-scale population declines. We also found possible signs of recent bottlenecks, perhaps resulting from forest clearing for dairy farming in the central part of the study area. This human disturbance also may have contributed to weak genetic structuring detected between the northeastern and northwestern part of the study area. Individual-based least cost path modeling showed limited influence of landscape variables on gene flow, with weak effects of variation in elevation in the northeast. In the northwest, however, landscape genetic models did not perform better than the null isolation-by-distance model. At the larger spatial scale of the northern part of the study area, elevation and temperatures were negatively correlated with gene flow, consistent with low dispersal suitability of higher elevation habitats that have lower temperatures and dense, wet vegetation. Overall, Tasmanian devils are a highly vagile species for which dispersal and gene flow appear to be influenced little by landscape features, and spread of devil facial tumor disease to the remaining portion of the devil’s geographic range seems imminent. Nonetheless, strong genetic structure found between the northern and southern portions of our study area, combined with low densities and limited possible colonization of DFTD from the east suggest there is some time for implementation of management strategies.

KW - Devil facial tumor disease

KW - Emerging infectious diseases

KW - Landscape genetics

KW - Tasmanian devil

UR - http://www.scopus.com/inward/record.url?scp=85019749493&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85019749493&partnerID=8YFLogxK

U2 - 10.1007/s10592-017-0980-4

DO - 10.1007/s10592-017-0980-4

M3 - Article

AN - SCOPUS:85019749493

VL - 18

SP - 1287

EP - 1297

JO - Conservation Genetics

JF - Conservation Genetics

SN - 1566-0621

IS - 6

ER -