An investigation of inbreeding depression and purging in captive pedigreed populations

“…size has been demonstrated empirically under controlled conditions (laboratory: Frankham 2005; Swindell & Bouzat 2006c; Wright et al. 2007; animals in captivity: Ralls et al. 1979; Ballou & Ralls 1982; Boakes et al. 2007) as well as in the wild (Crnokrak & Roff 1999; Keller & Waller 2002).”

“Other management approaches that have been recommended in conservation genetics are more controversial, such as purging inbreeding depression (Boakes et al. 2007) or supplementation of natural populations with captive-raised individuals (Ryman and Laikre 1991).”

“However, without genetic analyses it is not possible to assess the accuracy of studbook data (Boakes et al. 2007).”

“review of the experimental evidence by Crnokrak and Barrett (2002) and of studies from captive populations by Boakes et al. (2007) suggest, however, that purging may not be a strong force in small populations.”

“, ranging from 40–300 individuals, depending upon intensity of selection) and the mutations leading to inbreeding depression should be strongly deleterious and highly recessive [3, 7].”

“…alleles could have reduced inbreeding depression, but empirical studies suggest that purging is inefficient in small populations (Hedrick 1994; Wang 2000; Boakes et al. 2007), and that detrimental alleles may instead be randomly fixed by genetic drift, increasing the genetic load (Wang 2000).”

“…population size shrinks plays an important role on the evolution of different biological mechanisms that can allow populations to deal with their load, as diploidy, sexual reproduction, recombination, or breeding population structure (Charlesworth and Charlesworth 1987; Kondrashov and Crow 1991).”

“This load, when exposed by inbreeding, is responsible for at least part of the decline in fitness traits (inbreeding depression) ubiquitous in all captive populations and species at the verge of extinction (Hedrick and Kalinowski, 2000; Boakes et al., 2007; Charlesworth and Willis, 2009).”

“Particularly with respect to minimizing MK breeder selection protocols, pedigree-based methods have proven effective at minimizing the loss of genetic diversity (Lacy 2009) although inbreeding depression still occurs in some captive populations (Boakes et al. 2007).”

“For example, purging is now understood to be unreliable for mitigating inbreeding depression (Boakes et al., 2007; see also Lynch and Walsh, 1998).”

“…studies, both theoretical (Wang et al. 1999; Wang 2000; Whitlock 2002; Glémin 2003) and empirical (Bar- rett and Charlesworth 1991; Ballou 1997; Lacy and Ballou 1998; Byers and Waller 1999; Crnokrak and Barrett 2002; Boakes et al. 2007), have demonstrated that purging is not always effective.”

“Crnokrak & Roff 1999; Keller & Waller 2002) and the minimisation of inbreeding is a goal of many conservation programmes (e.g. Amos & Balmford 2001; Boakes et al. 2007).”

“This biases the regression of inbreeding on performance and therefore estimates of inbreeding depression may be regressed towards zero [10].”

“effect of genetic diversity loss and inbreeding depression in the wild is still uncertain (Boakes et al. 2007).”

“Other studies have previously reported that purging may not effectively reduce inbreeding depression in all traits (63, 64).”

“…purged within a consanguineous population because the selection efficiency against deleterious recessive alleles is increased by inbreeding (Hedrick, 1994; Ballou, 1997; Wang et al., 1999; Crnokrak and Barrett, 2002; Glémin, 2003; Boakes and Wang, 2005; Boakes et al., 2007; Garcı́a-Dorado, 2012).”

“Purging of deleterious alleles via inbreeding is often observed in captive animal populations, but its impact is relatively small and highly variable (Ballou 1997; Boakes et al. 2007).”

“Although empirical evidence for the effectiveness of purging is inconsistent (see e.g. Byers and Waller 1999; Crnokrak and Barrett 2002; Boakes et al. 2007; Leberg and Firmin 2008), some empirical studies do suggest that the relationship between population fitness and inbreeding level can be…”

“Theory predicts that recessive deleterious alleles – which when expressed in homozygotes are thought to be the main cause for inbreeding depression – can be purged from a population by selection [29,34,38,113–118].”

“Inbreeding is also not always avoided (Holand et al. 2007), perhaps because it may be innocuous unless if extreme or recurrent (e.g. Boakes et al. 2007).”

“Purging of the mutational load may alleviate this over time (Crnokrak & Barrett 2002), but its effectiveness in wild populations is uncertain (Boakes et al. 2007).”

“However, the outcomes of inbreeding are not always predictable (Boakes et al. 2006).”

“Finally, failing to detect inbreeding depression in juvenile survival of Stewart Island robins may be due to partial purging of the inbreeding load, via historical inbreeding and selection (Keller & Waller, 2002; Swindell & Bouzat, 2006b; Boakes et al., 2007; Bouzat, 2010).”

“However, given their often-small effective population size, the long-term viability of captive-bred populations is not guaranteed, and many show signs of inbreeding depression (Boakes et al., 2007).”

“Despite the effects of purging have often been considered weak or limited, to some extent supported by the apparent absence of purging (or weak purging) in several empirical analy‐ ses (Byers and Waller 1999; Reed et al. 2003a; Boakes et al. 2007), both theoretical and empirical results support that purging can be rel…”

“A review conducted on mammals, however, revealed contrasting results, with purging not substantially reducing inbreeding depression [15].”

“2001; Radwan 2003), and studies on captive populations of animals (Ballou 1997; Boakes et al. 2007).”

“The impact of increased individual homozygosity on individual fitness has been extensively documented in both laboratory, semi-natural, and natural settings [2,5-9].”

“The extent to which shifts in dominance are locus- and environment-specific may help to explain varying experimental results concerning purging (Byers & Waller 1999; Crnokrak & Barrett 2002; Boakes et al. 2007).”

“Captive populations are often small and consequently inbreeding rates can be high with associated reductions in fitness (Meuwissen and Woolliams, 1994; Boakes et al., 2007; Oldenbroek, 2007).”

“This corresponds to expectations that purging will not be efficient in a small population in which genetic drift may override weak to moderate selection (Hedrick 1994; Keller and Waller 2002; Glémin 2003; Boakes et al. 2007).”

“However, experimental evidence and investigations of captive populations have cast doubt on the existence or effectiveness of purging (Boakes et al. 2007; Leberg and Firmin 2008).”

“Nevertheless, experimental evidence supporting purging is limited, and studies often show that purging has limited success in reducing inbreeding depression in variable environments when applied to small populations (e.g., Ballou 1997; Jamieson et al. 2003; Boakes et al. 2007).”

“These results support the conclusion from e.g. Boakes et al. (2007) that purging cannot be used as a management tool in conservation biology.”

“We modelled four scenarios of (1) average management and (2) increased breeding management, as well as harvests under (3) average management and (4) increased breeding management.”

“Despite the acknowledged importance that purging can have on inbreeding depression, the occurrence and efficiency of purging remain actively debated (Ballou, 1997; Byers & Waller, 1999; Crnokrak & Barrett, 2002; Boakes et al., 2007).”

“For example, inbreeding can contribute to declines in breeding success in conservation programs (Boakes et al. 2007), although variation in pedigree-based inbreeding metrics was too low to include these parameters in our analyses of devil.”

“In ephemeral habitats, migration is necessary for populations to persist (see Denno et al. 1991), while in more stable habitats, not only is gene flow unnecessary, but limited gene flow can allow populations to diverge by chance alone (Wright 1968).”

“As a result, the expected effect on lowering fitness would be less than that from one-generation inbreeding of the same level because of the opportunity for purging of detrimental variants (Hedrick 1994; Boakes et al. 2007).”

“The efficiency of inbreeding to reduce d has been studied by analysing fitness in pedigreed data from cattle breeds and from zoo endangered populations (Boakes et al., 2007; Gulisija & Crow, 2007).”

“This highlights the long-term genetic impact of founder events, where small initial populations continue to affect diversity despite in-breeding management (Boakes et al. 2007).”

“…benefits of inbreeding (Kokko & Ots 2006), empirical evidence is in clear favour of inbreeding avoidance (Pusey & Wolf 1996; Keller & Waller 2002; Kruuk et al. 2002; Armbruster & Reed 2005; O’Grady et al. 2006; Boakes et al. 2007; but see Pusey & Wolf 1996 for studies that failed to show it).”

“…Conservation Partnership, Ohio State University, 300 Aronoff Laboratory, 318 West 12th Avenue, Columbus, OH 43210-1293, USA J. E. Chiucchi Center for Life Sciences Education, Ohio State University, 260 Jennings Hall, 1735 Neil Avenue, Columbus, OH 43210-1293, USA 2001; Boakes et al. 2007).”

“Significant effects of purging have been repeatedly reported for plants and animals (see the recent survey by Gulisija and Crow 2007) but attempts to empirically derive a predictive approach of its magnitude have proved elusive (Boakes et al. 2007).”

“[8] argued against this practice in zoo populations of threatened species in spite of finding evidence of purging in some of the populations they studied (see [9] for a review).”

“The influence of captive breeding on the genetic diversity of endangered species has already been subject to a number of theoretic and genetic studies [7,14–16,17].”

“…due to reduced genetic load (i.e. genetic purging) are thought to be rather restrictive in natural populations, and supporting evidence for purging in wild or even captive populations is contentious (Byers and Waller 1999, Crnokrak and Barrett 2002, Keller and Waller 2002, Boakes et al. 2007).”

“…survival are well documented in wild (Crnokrak and Roff, 1999; Hedrick and Kalinowski, 2000) and captive populations (Kristensen and Sørensen, 2005; Boakes et al., 2007), but no overall correlation between inbreeding, microsatellite heterozygosity, and mean squared allelic distance (d2) in…”

“There are considerable risks associated with such reintroductions, including potential inbreeding de fi cits (Boakes et al., 2007; Leberg and Firman, 2007), a lack of clarity regarding the genetic origin of captive animals (Williams et al., 2021), elevated risks that they are habituated to humans…”

“Purging tends to regress inbreeding depression towards zero because homozygosity in some genomic regions is no longer unfavourable (Boakes et al., 2007).”

“In addition, although there have been few studies considering the effects of parental inbreeding (e.g. Ballou, 1997; Boakes et al., 2007), they commonly use the individual inbreeding coefficient as the predictor variable (Kalinowski, Hedrick & Miller, 1999).”

“…effect of inbreeding on ‘Alalā offspring survival suggests that genetic purging of recessive deleterious alleles in the population is incomplete and that allelic diversity remains (Weiser et al. 2015), despite the likely occurrence of ancestral inbreeding (Boakes et al. 2007; Sutton et al. 2018).”

“However, captive populations often begins with a small 89 number of individuals distributed in several breeding centers, partly due to spatial constraints 90 (Laikre 1999; Boakes et al. 2007), and if left unmanaged genetic drift and non-random 91 matings results in a rapid loss of genetic diversity and accumulation of…”

“It may also indicate an accumulation of genetic load due to relaxed selection, which may ultimately result in inbreeding depression (Boakes et al. 2006 ).”