Correcting parentage relationships in the endangered California Condor: Improving mean kinship estimates for conservation management

Abstract

Maintaining the existing biodiversity of endangered species is a goal of conservation management programs, and a major component of many collaborative efforts undertaken by zoos, field biologists, and conservation scientists. Over the past 3 decades, the San Diego Zoo has performed long-term genetic studies in support of the recovery program for the critically endangered California Condor (Gymnogyps californianus). This work has included sex determination of hatchlings and parentage confirmation using microsatellite genotyping. This paper describes the genetic work associated with the California Condor recovery program, which aims to provide a highly accurate pedigree for making informed captive pairing and release recommendations. Initial genotyping began after reintroduced California Condors started reproducing, and the focus was on birds hatched from their wild-laid eggs. However, genetic analysis showed discrepancies relative to behavioral observations of wild birds and led to the species-wide testing of all available samples. This genetic study has resolved instances of individual misidentifications and parental misassignments, verified the first cases of extra-pair paternity in this species, identified parentage where chicks were observed being raised by trios, and found 2 apparent de novo mutations in the captive condor population. Correcting the California Condor pedigree according to genetic parental analysis has produced more accurate estimates of mean kinship values among living birds, ranking potential breeders according to their actual breeding value and helping managers to make informed decisions about captive pairing and release of condors in the wild.

Average kinship within bighorn sheep populations is associated with connectivity, augmentation, and bottlenecks

“…Its utility has been verified in Drosophila experiments (Montgomery et al, 1997), and biologists use mean kinship to make breeding decisions for threatened species in captivity and rare domestic livestock breeds (Ballou et al, 2010; Falconer & Mackay, 1996; Frankham et al, 2010). Mean kinship is used to make breeding decisions to minimize inbreeding in most, if not all, wildlife captive‐breeding programs to support reintroductions, including for the black‐footed ferret ( Mustela nigripes ) and California condor ( Gymnogyps californianus ; Ballou & Foose, 1996; Moran et al, 2021; Ralls & Ballou, 2004; Russell et al, 1994). Based on the fact that kinship is expected to be 0.125 for a second‐degree relationship (i.e., half‐siblings) and 0.0625 for a third‐degree relationship (i.e., first cousins), Frankham et al (2017) recommended that populations have a mean kinship value less than 0.1 to avoid inbreeding depression (Frankham et al, 2017; Manichaikul et al, 2010; Van Dyke, 2008).…”

Expanding the conservation genomics toolbox: Incorporating structural variants to enhance genomic studies for species of conservation concern

“…For example, individuals that carry, or express, negative fitness traits can be assessed in conservation breeding programs, followed by appropriate actions or recommendations (e.g., Attwater's prairie chicken; Hammerly et al, 2013 ). Alternatively, when inheritance of these traits are known, individuals may be screened prior to selective pairing (e.g., California Condor; Moran et al, 2021 ). Regardless, as we learn more about the mechanisms underlying fitness traits, especially traits associated with negative fitness, there is a pressing need to establish comprehensive evidence‐based management strategies that mitigate the impact of these traits while minimizing the loss of genome‐wide diversity.…”

“…Similarly, a large inversion resulting in a supergene underlies significant morphological and behavioural differences among white‐striped and tan‐striped morphs in White‐throated sparrows, with aggressiveness being monogenic in the white‐striped morph (Merritt et al, 2020 ). Although many fitness traits are likely to be polygenic, including traits of conservation interest such as disease susceptibility, reduced fertility and developmental abnormalities (e.g., Moran et al, 2021 ; Murchison et al, 2012 ; Roelke et al, 1993 ; Savage et al, 2020 preprint), those impacted by supergenes are likely to have relatively simple inheritance patterns which will enable their characterization and management.…”

“…Alternatively, when inheritance of these traits are known, individuals may be screened prior to selective pairing (e.g., California Condor; Moran et al, 2021). Regardless, as we learn more about the mechanisms underlying fitness traits, especially traits associated with negative fitness, there is a pressing need to establish comprehensive evidence-based management strategies that mitigate the impact of these traits while minimizing the loss of genome-wide diversity.…”

The relevance of pedigrees in the conservation genomics era

“…For relatively diverse wild populations, microsatellite‐based approaches can be informative (McLennan et al, 2018 ), especially for inferring close relatives. For example, a recent study from Moran et al, ( 2021 ) highlighted the benefit of using microsatellite markers to verify parentage in critically endangered California condor ( Gymnogyps californianus ). While microsatellites are useful, high density single nucleotide polymorphisms (i.e., SNPs) generated through high throughput sequencing approaches (i.e., HTS) often provide better resolution for estimating identity‐by‐descent, even when populations are inbred or relationships are more distant (Allendorf et al, 2010 ; Flanagan & Jones, 2019 ; Galla et al, 2020 ; Taylor, 2015 ).…”