Founder relationships and conservation management: empirical kinships reveal the effect on breeding programmes when founders are assumed to be unrelated

Abstract

Conservation breeding programmes have become widespread as natural habitats shrink, and have been historically managed using pedigree data and an assumption that population founders are unrelated. Molecular genotyping is able to determine founder relatedness, but is rarely used. To empirically test the impact of assuming founders to be unrelated, we utilized data from 203 founding individuals and 11 subsequent years of breeding records for the Tasmanian devil (Sarcophilus harrisii) insurance population. We integrated molecular data (N = 119 founders) and detailed trapping information (N = 203 founders) to test how founder relationship assumptions impacted the genetic characteristics of the population over time (N = 942 unique individuals). We developed a method to combine molecular kinship (using the TrioML estimator), year of birth and trapping location, and integrated the resulting empirical kinship estimates into population management software. We tested the effect of using pedigree data only, versus our integrated approach, on population outcomes. Inbreeding coefficients evaluated using the integrated approach were significantly higher than pedigree-only inbreeding coefficients in the first few years following population establishment. A geographic distanceonly approach showed an association between kinship and probability of successful breeding. Our results show the value in using field and/or molecular data combined with pedigree data in conservation breeding programmes to provide new information for managing crucial populations and improving their success. We caution population managers against commencing expensive conservation breeding programmes in the absence of understanding founder relatedness, especially when wild augmentation is a goal. Long-term costs of assuming founders are unrelated include financial costs, reduced productivity and release of potentially highly inbred individuals.

A comparison of pedigree, genetic and genomic estimates of relatedness for informing pairing decisions in two critically endangered birds: Implications for conservation breeding programmes worldwide

“…Still, it should be noted that many pairs with pedigree-based relatedness values of 0 had SNP-based relatedness values ranging upwards of 0.40 in kakī 0.33 and in kākāriki karaka, which approximates first-and second-order relationships in both species (Figure 2). This indicates that pedigree-based R between these individuals may be downwardly biased by the assumption that no variance in relatedness exists among founders, missing information and/or low pedigree depth (Balloux et al, 2004;Bérénos et al, 2014;Hammerly et al, 2016;Hogg et al, 2019;Kardos et al, 2015;Lacy, 1995;Pemberton, 2008;Rudnick & Lacy, 2008;Tzika et al, 2009).…”

A comparison of pedigree, genetic, and genomic estimates of relatedness for informing pairing decisions in two critically endangered birds

“…Still, it should be noted that many pairs with pedigree-based relatedness values of 0 had pairwise relatedness values ranging upwards of 0.40 in kakī 0.33 and in kākāriki karaka using a SNPbased approach, which approximates first and second order relationships in both species (Figure 2). This indicates that pedigree-based R between these individuals may be downwardly biased by unknown founders, missing information, and/or low pedigree depth (Balloux et al, 2004;Bérénos et al, 2014;Hammerly et al, 2016;Hogg et al, 2018;Lacy, 1995;Pemberton, 2008;Rudnick & Lacy, 2008;Tzika et al, 2009).…”

“…While pedigrees are still considered the 'gold standard' for estimating relatedness in conservation breeding programmes (Hammerly, de la Cerda, Bailey, & Johnson, 2016;Jiménez-Mena, Schad, Hanna, & Lacy, 2016), there are inherent assumptions that, when violated, hinder pedigree accuracy. For example, pedigrees assume that all founders are unrelated (Ballou, 1983), which is unlikely for many highly threatened wild populations, given most will have experienced one or more historical population bottlenecks and founders sourced from these remnant wild populations are likely related (Bergner, Jamieson, & Robertson, 2014;Hogg et al, 2018). Simulation studies suggest that complete pedigrees with substantial depth (> 5 generations recorded) are robust enough to reflect true relatedness and inbreeding estimates despite violating this assumption (Balloux, Amos, & Coulson, 2004;J.…”

“…Under these circumstances, pedigree depth may remain perpetually shallow and therefore susceptible to violations of the assumption of founder relatedness. This is captured by Hogg et al (2018), who demonstrate how violating this assumption led to a significant underestimation of both relatedness and inbreeding in a conservation breeding programme routinely augmented by wild individuals. In addition to these caveats, many intensively managed populations are poorly pedigreed, meaning these pedigrees contain missing information (i.e., unknown parentage due to matings that include unidentified individuals or extra-pair parentage; Bérénos, Ellis, Pilkington, & Pemberton, 2014;Lacy, 2009;Pemberton, 2008;Putnam & Ivy, 2014) or record keeping errors (e.g., Hammerly et al, 2016).…”

Genetic Management of Captive and Reintroduced Bilby Populations

“…The rate at which heterozygosity is lost from a population will be further influenced by the sex ratio of breeding individuals, interspecific variation in offspring numbers, generation times, and the mating system of the specific threatened species in question (Amos and Harwood , Jamieson and Lacy ). It is therefore important that stakeholders employ active genetic monitoring to guide and evaluate the management of genetic diversity as part of captive breeding efforts and following translocation events (Schwartz et al , Hogg et al ).…”