Inbreeding depression in one of the last DFTD-free wild populations of Tasmanian devils

Abstract

Background Vulnerable species experiencing inbreeding depression are prone to localised extinctions because of their reduced fitness. For Tasmanian devils, the rapid spread of devil facial tumour disease (DFTD) has led to population declines and fragmentation across the species’ range. Here we show that one of the few remaining DFTD-free populations of Tasmanian devils is experiencing inbreeding depression. Moreover, this population has experienced a significant reduction in reproductive success over recent years. Methods We used 32 microsatellite loci to examine changes in genetic diversity and inbreeding in the wild population at Woolnorth, alongside field data on breeding success from females to test for inbreeding depression. Results Wefound that maternal internal relatedness has a negative impact on litter sizes. The results of this study imply that this population may be entering an extinction vortex and that to protect the population genetic rescue should be considered. This study provides conservation managers with useful information for managing wild devils and provides support for the “Wild Devil Recovery Program”, which is currently augmenting small, isolated populations.

Restoring faith in conservation action: Maintaining wild genetic diversity through the Tasmanian devil insurance program

“…Breeding success varies across the range ( Farquharson et al., 2018 ; Guiler, 1970 ), with DFTD-affected populations experiencing precocial breeding ( Jones et al., 2008 ; Lachish et al., 2009 ). Previous studies have noted reductions in reproductive success at Woolnorth, a western DFTD-free population included in this study and impacted by inbreeding depression ( Farquharson et al., 2018 ; Gooley et al., 2020 ). Reproductive genes of interest identified through our method are a useful starting point for investigating reproductive failure and variation in reproductive patterns across the range.…”

“…We applied both a reduced representation sequencing method to generate 1,819 genome-wide SNPs from 1,383 Tasmanian devils and a custom target capture method to examine functional diversity at 556 genes and 53 putative DFTD-associated loci. Previous studies of Tasmanian devils have investigated population structure at various locations using between 10 and 42 microsatellite markers ( Storfer et al., 2017 ; Brüniche-Olsen et al., 2013 , 2014 ; McLennan et al., 2018 ; Grueber et al., 2018 ; Lachish et al., 2011 ; Jones et al., 2004 ; Gooley et al., 2020 ), using SNPs from 7 locations ( Fraik et al., 2020 ), or using SNPs at 38 locations but with only 1–2 samples per site ( Hendricks et al., 2017 ). We found previously unreported evidence of fine-scale genetic structuring ( Miller et al., 2011 ), reflective of biogeographic patterns ( Figures 1 C and 1D).…”

“…Although DFTD is a significant threatening process for Tasmanian devils, other threatening processes exist including significantly reduced population densities ( Lazenby et al., 2018 ), evidence of inbreeding ( Grueber et al., 2018 ), evidence of inbreeding depression ( Gooley et al., 2020 ), roadkill ( Lawrence and Weirsma, 2019 ), and a fragmented landscape. Translocations are a recognized conservation tool to minimize the risk of extinction from small population pressures and improve gene flow ( Frankham et al., 2017 ).…”

“…The DFTD naive argument for the insurance metapopulation ( Hamede et al., 2021 ) appears to be unfounded, as the DFTD-associated loci are present at similar allele frequencies in the IP and the wild. Due to the high heterozygosity observed in the insurance metapopulation and its overall representation of species’ genetic diversity, sourcing devils from these populations for translocations may alleviate the impacts of inbreeding ( Gooley et al., 2020 ), introduce new alleles, and assist with gene flow ( Allendorf et al., 2012 ). For species whose threatening process cannot be successfully mitigated in the wild, understanding whether insurance populations are representative of wild diversity is essential to long-term management.…”

Conservation Biology and Reproduction in a Time of Developmental Plasticity

“…A relevant, and outstanding, example of the care that would be needed involves attempts to conserve the Tasmanian devil ( Sarcophilus harrisii ). This Australian carnivorous marsupial is under considerable threat from inbreeding depression [ 92 ], as well as a contagious and fatal form of facial tumour. In 2012, an insurance subpopulation of uninfected animals, derived from two separate founder populations, was established on Maria Island, Tasmania, as one of the conservation measures.…”