Tracing the rise of malignant cell lines: Distribution, epidemiology and evolutionary interactions of two transmissible cancers in Tasmanian devils.

Samantha James,Andrew Storfer,Paul A Hohenlohe,Samantha Fox,Young Mi Kwon,Frédéric Thomas,Hamish Mccallum,David Pemberton,Rodrigo Hamede,Geordie Jennings,Elizabeth P Murchison,Ruth J Pye ,Maximilian R Stammnitz ,A Bruce Lyons ,B N Brown ,Menna Lloyd Jones ,Sébastien Comte ,Beáta Újvári ,Hannah V Siddle ,Alexandra K Fraik ,Gregory M Woods

doi:10.1111/eva.12831

Abstract

Emerging infectious diseases are rising globally and understanding host‐pathogen interactions during the initial stages of disease emergence is essential for assessing potential evolutionary dynamics and designing novel management strategies. Tasmanian devils (Sarcophilus harrisii) are endangered due to a transmissible cancer—devil facial tumour disease (DFTD)—that since its emergence in the 1990s, has affected most populations throughout Tasmania. Recent studies suggest that devils are adapting to the DFTD epidemic and that disease‐induced extinction is unlikely. However, in 2014, a second and independently evolved transmissible cancer—devil facial tumour 2 (DFT2)—was discovered at the d’Entrecasteaux peninsula, in south‐east Tasmania, suggesting that the species is prone to transmissible cancers. To date, there is little information about the distribution, epidemiology and effects of DFT2 and its interaction with DFTD. Here, we use data from monitoring surveys and roadkills found within and adjacent to the d’Entrecasteaux peninsula to determine the distribution of both cancers and to compare their epidemiological patterns. Since 2012, a total of 51 DFTD tumours have been confirmed among 26 individuals inside the peninsula and its surroundings, while 40 DFT2 tumours have been confirmed among 23 individuals, and two individuals co‐infected with both tumours. All devils with DFT2 were found within the d’Entrecasteaux peninsula, suggesting that this new transmissible cancer is geographically confined to this area. We found significant differences in tumour bodily location in DFTD and DFT2, with non‐facial tumours more commonly found in DFT2. There was a significant sex bias in DFT2, with most cases reported in males, suggesting that since DFT2 originated from a male host, females might be less susceptible to this cancer. We discuss the implications of our results for understanding the epidemiological and evolutionary interactions of these two contemporary transmissible cancers and evaluating the effectiveness of potential management strategies.

Highlights

Emerging infectious diseases are becoming a critical concern for wildlife conservation, livestock and public health (Daszak, Cunningham, & Hyatt, 2000; Johnson, Roode, & Fenton, 2015; Jones et al, 2008)
A trial of selective culling to eradicate a transmissible cancer on the Forestier peninsula in south‐east Tasmania was unsuccessful (Lachish, McCallum, Mann, Pukk, & Jones, 2010), and modelling suggested that no feasible rate of culling infected animals would be successful in eradicating the disease (Beeton & McCallum, 2011)
We acknowledge that a larger sampling effort in areas north of the peninsula is necessary to firmly conclude that devil facial tumour 2 (DFT2) has not escaped the confinement of the peninsula; our estimates of current distribution should be interpreted with caution

Summary

| INTRODUCTION

Emerging infectious diseases are becoming a critical concern for wildlife conservation, livestock and public health (Daszak, Cunningham, & Hyatt, 2000; Johnson, Roode, & Fenton, 2015; Jones et al, 2008). Transmission occurs via direct inoculation of live tumour cells when devils bite each other (Hamede, McCallum, & Jones, 2013; Pearse & Swift, 2006). Co‐infection with DFTD and DFT2 has been reported in the same host (Kwon et al, 2018); competition and selective processes between these two transmissible tumours are expected both at individual and population levels. A better knowledge of the interaction between these two transmissible cancers might allow the evaluation of potential epidemiological and evolutionary dynamics between devils, DFTD and DFT2, and assess whether management interventions are required. We discuss the implications of our study for evaluating the epidemiological and evolutionary interactions of the two transmissible cancers and discuss the effectiveness of potential management and disease control strategies

| MATERIALS AND METHODS

Findings

| DISCUSSION