Abstract

Inbreeding threatens the survival of small populations by producing inbreeding depression, but also exposes recessive deleterious effects in homozygosis allowing for genetic purging. Using inbreeding-purging theory, we analyze early survival in four pedigreed captive breeding programs of endangered ungulates where population growth was prioritized so that most adult females were allowed to contribute offspring according to their fitness. We find evidence that purging can substantially reduce inbreeding depression in Gazella cuvieri (with effective population size Ne = 14) and Nanger dama (Ne = 11). No purging is detected in Ammotragus lervia (Ne = 4), in agreement with the notion that drift overcomes purging under fast inbreeding, nor in G. dorcas (Ne = 39) where, due to the larger population size, purging is slower and detection is expected to require more generations. Thus, although smaller populations are always expected to show smaller fitness (as well as less adaptive potential) than larger ones due to higher homozygosis and deleterious fixation, our results show that a substantial fraction of their inbreeding load and inbreeding depression can be purged when breeding contributions are governed by natural selection. Since management strategies intended to maximize the ratio from the effective to the actual population size tend to reduce purging, the search for a compromise between these strategies and purging could be beneficial in the long term. This could be achieved either by allowing some level of random mating and some role of natural selection in determining breeding contributions, or by undertaking reintroductions into the wild at the earliest opportunity.

Highlights

  • The decline in fitness due to inbreeding is one of the major threats menacing the survival of small, endangered populations (Lande 1994; Hedrick and Kalinowski 2000; Crow 2008; Frankham 2010; Frankham et al 2014a)

  • Tm assumed constant population size, comparing these values with the corresponding EqG suggests that the period studied is too short for purging to be detected in the case of G. dorcas

  • All these results suggest that population management performed with G. cuvieri and in A. lervia at La Hoya preserved their genetic diversity better than in the other two species

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Summary

Introduction

The decline in fitness due to inbreeding is one of the major threats menacing the survival of small, endangered populations (Lande 1994; Hedrick and Kalinowski 2000; Crow 2008; Frankham 2010; Frankham et al 2014a). Large populations harbor many (partially) recessive deleterious mutations segregating at low frequency whose effects hide in heterozygosis but, under inbreeding, increase their expression in homozygosis (Charlesworth and Willis 2009) This exposure of recessive effects produces inbreeding depression and causes an enhancement of natural selection that has been referred to as genetic purging (Crow 1970; Hedrick 1994) and that can substantially reduce both inbreeding depression and inbreeding load (Wang and Hill 1999; García-Dorado 2012; Charlesworth 2018). Genetic purging has received less attention than inbreeding depression in the literature (Keller and Waller 2002; Bouzat 2010; Hedrick and García-Dorado 2016) as it is more difficult to detect This is partly because it is expected to be more successful and slower under slower inbreeding, so that a large number of generations may be required before the effects of purging become apparent (García-Dorado 2012; López-Cortegano et al 2018). Purging has rarely been documented in nature (Byers and Waller 1999; Crnokrak and Barrett 2002) and many studies aimed to detect genetic purging have failed or found inconsistent results among species, both in captive and wild populations (Ballou 1997; Boakes et al 2007; Leberg and Firmin 2008; Kennedy et al 2014)

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