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

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 heterozygosityfitness 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.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 . In 2006, Australia's largest insurance metapopulation was established under management of the Save the Tasmanian Devil Program (STDP), in collaboration with the Zoo and Aquarium Association (ZAA), to breed Tasmanian devils away from the disease for ultimate release back into the wild 2 . Preservation of the genetic diversity of the species is critical and, at its establishment, the insurance population aimed to maintain 95% of genetic diversity over 50 years. Within the Tasmanian devil insurance population (and also in many other insurance populations for other species) the relationship of the founding individuals was unknown.The insurance metapopulation was seeded by a total of 122 founders collected over four intakes from 2005 to 2008 3 . Young, dispersing juveniles were sourced and combined with the existing captive population of 112 animals, originating from 25 genetic founders 4 (for a review and map of recent and pre-existing founder provenance see ref.2). At the time of collection, the rapid spread of DFTD across the island of Tasmania resulted in devils being preferentially sourced from the north-west of Tasmania, as populations there were disease-free (see ref.3). Despite best efforts, it is possible that some of the initial founding animals were closely related (accounting for dispersal patterns of Tasmanian devils and founder collection locations 2, 3 ). As founder intakes were weighted to two specific regions (see map 2 ), and Ta...

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