No outbreeding depression in a trial of targeted gene flow in an endangered Australian marsupial

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RESEARCH ARTICLE

No outbreeding depression in a trial of targeted gene flow in an endangered Australian marsupial Ella Kelly1   · Kenbi Traditional Owners and Rangers2 · Chris J. Jolly1   · Naomi Indigo3   · Adam Smart1   · Jonathan Webb3   · Ben Phillips1  Received: 15 May 2020 / Accepted: 13 October 2020 © Springer Nature B.V. 2020

Abstract Targeted gene flow is a novel conservation strategy that involves translocating individuals with favourable genes to areas where they will have a conservation benefit. One oft-cited risk of the strategy is the potential for outbreeding depression. Here, we used the northern quoll (Dasyurus hallucatus) as a model to test this possibility for the first time in a field setting. Northern quolls are endangered by the spread of the invasive cane toad (Rhinella marina), which they are fatally poisoned by, if they mistakenly attempt to consume them. There are, however, a small number of quolls that are “toad-smart”—they possess a heritable trait that means they innately do not attack toads. It is this trait we hoped to promote through targeted gene flow. We established a hybrid population (54 toad-smart and toad-naïve northern quolls) and introduced this population onto a small offshore, toad-infested island in 2017. Genetic data suggests an increase in the toad-smart proportion of the genome increasing from 29.4% in the release population to 40.2% in the first island generation (F2). Our data demonstrate successful in situ hybridisation between populations, with viable F2 hybrids and backcrosses observed, and some evidence of heterosis (hybrid vigour) in F1 hybrids. The population experienced significant reductions in size over the two years, however, through a combination of toad-mortality, as well as stochastic processes including fire, a cyclone, predation and ineffective breeding, and so small sample sizes hamper our results. Such establishment problems would not occur were we to attempt targeted gene flow into already established quoll populations, and our observation of successful hybridisation suggests targeted gene flow could be a viable strategy in established quoll populations soon to be impacted by toads. Keywords  Assisted gene flow · Evolutionary rescue · Trait variation · Rhinella marina · Dasyurus hallucatus

Introduction In a climate of rapid environmental change and widespread biodiversity decline, conservationists are racing to devise effective strategies to conserve threatened species (Johnson Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s1059​2-020-01316​-z) contains supplementary material, which is available to authorized users. * Ella Kelly [email protected] 1



School of Biosciences, The University of Melbourne, Parkville, VIC, Australia

2



Kenbi Traditional Owners and Rangers, Cox Peninsula, NT, Australia

3

School of Life Sciences, University of Technology Sydney, Sydney, NSW, Australia



et al. 2017). Conservationists face numerous interacting challenges, including habitat loss, clima