No evidence of inbreeding depression in a Tasmanian devil insurance population despite significant variation in inbreeding

Rebecca Gooley,Carolyn J Hogg,Katherine Belov,Catherine E Grueber

doi:10.1038/s41598-017-02000-y

Rebecca Gooley, Carolyn J Hogg + Show 2 more

Open Access

https://doi.org/10.1038/s41598-017-02000-y

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Abstract

Inbreeding depression occurs when inbred individuals experience reduced fitness as a result of reduced genome-wide heterozygosity. The Tasmanian devil faces extinction due to a contagious cancer, devil facial tumour disease (DFTD). An insurance metapopulation was established in 2006 to ensure the survival of the species and to be used as a source population for re-wilding and genetic rescue. The emergence of DFTD and the rapid decline of wild devil populations have rendered the species at risk of inbreeding depression. We used 33 microsatellite loci to (1) reconstruct a pedigree for the insurance population and (2) estimate genome-wide heterozygosity for 200 individuals. Using heterozygosity-fitness correlations, we investigated the effect of heterozygosity on six diverse fitness measures (ulna length, asymmetry, weight-at-weaning, testes volume, reproductive success and survival). Despite statistically significant evidence of variation in individual inbreeding in this population, we found no associations between inbreeding and any of our six fitness measurements. We propose that the benign environment in captivity may decrease the intensity of inbreeding depression, relative to the stressful conditions in the wild. Future work will need to measure fitness of released animals to facilitate translation of this data to the broader conservation management of the species in its native range.

Highlights

The Tasmanian devil (Sarcophilus harrisii), the largest extant carnivorous marsupial, faces extinction due to the emergence of a contagious cancer called Devil Facial Tumour Disease (DFTD)[1]
Short-term consequences (3 to 5 generations) of an initial increase in inbreeding values were exposed when founders were assumed to be unrelated compared to a model of known founder relationships and inbreeding[7]. This finding highlights the importance of understanding the recent ancestry of founders when commencing an insurance population, those which will be used for rewilding and genetic rescues soon after instigation, such as in the case of the Tasmanian devil insurance population
We investigated whether female mate choice was for the most heterozygous male per enclosure, or alternatively, if female mate choice had a heterozygosity threshold

Summary

Introduction

The Tasmanian devil (Sarcophilus harrisii), the largest extant carnivorous marsupial, faces extinction due to the emergence of a contagious cancer called Devil Facial Tumour Disease (DFTD)[1]. Short-term consequences (3 to 5 generations) of an initial increase in inbreeding values were exposed when founders were assumed to be unrelated compared to a model of known founder relationships and inbreeding[7] This finding highlights the importance of understanding the recent ancestry of founders when commencing an insurance population, those which will be used for rewilding and genetic rescues soon after instigation, such as in the case of the Tasmanian devil insurance population. At least three population crashes, resulting in genetic bottlenecks, have been documented in Tasmania since devils were isolated on the island approximately 10,000 years ago[11] Most recently, this species has suffered an extreme population decline (~85%)[12] due to the emergence of two transmissible cancer lines, Devil Facial Tumour 1 (DFT1) and Devil Facial Tumour 2 (DFT2), first documented in 1996 and 2015 respectively[13, 14]. These severe population declines have rendered the Tasmanian devil at risk of further genetic diversity loss and inbreeding depression

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