Pedigrees in conservation management
Pedigrees have been particularly well suited for the genetic management of captive (ex situ ) or intensively managed wild (in situ ) or semi-wild (‘sorta’ situ ; Wildt et al., 2019) populations of animals and plants, where ancestry is more easily documented. Pedigree use is exemplified by the zoo and aquarium community, who have built a data-driven paradigm of pedigree-based management, including user-friendly software to manage pedigree information (e.g., SPARKS, PopLink, ZIMS; Faust et al., 2021, Species 360) and to calculate pedigree-based genetic statistics (e.g., PMx, Lacy, Ballou, & Pollak, 2012). Pedigree-based conservation management is often kinship-based, with the coefficient of kinship (f ) being a metric of the coefficient of relatedness (R, R = 2f in the absence of inbreeding; Lacy, 2005, 2009). Common pedigree-based statistics for small population management include mean kinship (i.e., MK, or the average kinship of one individual to all others in a population, including oneself), inbreeding coefficients (F ), and population-level gene diversity (GD, also known as expected heterozygosity; Ballou et al., 2010). These statistics are regularly used to minimize mean kinship and inbreeding in threatened populations to maintain the evolutionary potential of the species of interest (Ivy, Miller, Lacy, & DeWoody, 2009; Willougby et al., 2015; Galla et al., 2020). Indeed, studies have shown the efficacy of this approach (Lacy, 2009), with pedigrees being used to measure and manage diversity and inbreeding in animals worldwide, including Atlantic and sockeye salmon (Salmo salar and Oncorhynchus nerka , respectively; O’Reilly & Kozfkay, 2014), Tasmanian devil (Sarcophilus harrisii ; McLennan et al., 2018; Wright, Hogg, McLennan, Belov, & Grueber, 2021), American bison (Bison bison ; Giglio et al., 2016, 2018), whooping crane (Grus americana ; Boardman, Mace, Peregoy, & Ivy, 2017), takahē (Porphyrio hochstetteri ; Grueber & Jamieson, 2008) and Houbara bustard (Chlamydotis undulata undulata ; Rabier, Robert, Lacroix, & Lesobre, 2020). When pedigrees are complete and accurate, they have been shown to explain more variation in inbreeding than microsatellites (Nietlisbach et al., 2017) and provide similar estimates of relatedness to thousands to tens of thousands of genome-wide single nucleotide polymorphisms (i.e., SNPs; Galla et al., 2020). While pedigrees have been extensively used to manage genome-wide diversity of animals in zoos and aquaria, a recent review by Wood et al., (2020) has highlighted their potential for managing diversity and viability for plant collections and seed banks. Ongoing efforts are being made to optimize collections and maintain plant material ex situ for long-term conservation and potential use in future restoration (Di Santo & Hamilton, 2020). The goals of these collections are to both preserve diversity representative ofin situ population differences across a species’ range, and to ensure that ex situ population genetic variation is maintained to preserve adaptive evolutionary potential (Di Santo & Hamilton, 2020; Hamilton et al., 2020). Given the overlapping goals —but differing approaches— of plant and animal conservation breeding programs, we anticipate that zoo, aquaria, and botanical communities will learn much from one another as different approaches are developed and tested.
Most zoos and aquaria use pedigrees in a well-supported paradigm of measuring and managing putatively neutral genome-wide diversity, but pedigrees have also been used to characterize and manage functional diversity within ex situ plant and fisheries systems. For example, in 1983 the American Chestnut Foundation embarked on an ambitious breeding program to backcross blight-susceptible American chestnut (Castanea dentata ) —a species on the brink of extinction— with blight-resistant Chinese chestnut (C. mollisima ). In this instance, ancestry data from pedigrees and phenotypic data on blight resistance were used for crossing programs, based on the hypothesis that blight resistance had a genetic basis (Scheiner et al., 2017; Westbrook et al., 2020). In addition to disease resistance, pedigrees are often used in greenhouses or intensively managed common gardens to understand the functional ability of plants to cope with stress through gene-by-environment (i.e., GxE) experiments (e.g., George et al., 2020). These experiments aim to disentangle genetic (as derived from pedigree-based kinship) and environmental contributions, and their interactions, to explain phenotypes of interest in individuals. Conservation biologists can then use predictions of local environmental conditions in the short- to medium-term to select well-adapted individuals or varieties for conservation translocations and restoration (e.g., Richardson & Chaney, 2018).
Pedigree data has also advanced our understanding of wild populations and ability to manage them (i.e., in situ or sorta situconservation; Kruuk & Hill, 2008; Wildt et al., 2019). For a pedigreed natural population of Florida scrub jays (Aphelocoma coerulescens ), researchers used pedigrees to predict the effects of selection and gene flow on how declining populations might evolve in a short time period (Chen et al., 2019). A wild pedigree for gray wolves (Canus lupus ) in Yellowstone National Park combined with phenotypes recorded for those individuals led to advances in understanding the heritability of behaviour and the genetic basis of mange in this iconic species (Von Holdt et al., 2019; DeCandia, Schrom, Brandell, Stahler, & von Holdt, 2021). Pedigrees have also been used in Eastern Massasauga rattlesnakes (Sistrurus catenatus ) to elucidate dispersal and connectivity between populations, with implications for restoration and translocation efforts (Martin et al., 2021). Important to conservation efforts for small and isolated wild populations, is the ability to re-establish gene flow using conservation translocations (i.e., genetic rescue; Ralls, Sunnucks, Lacy, & Frankham, 2020). Documented ancestry of wild populations can help refine estimates of effective population size, social group structure, genetic connectivity among populations, and potential local adaptation amongst populations, which can aid in designing successful translocation programs that minimize inbreeding depression while avoiding outbreeding depression. For example, pedigrees have been used to inform genetic conservation or rescue efforts for wild populations of black-tailed prairie dogs (Cynomys ludovicianus ; Shier 2006), Rocky Mountain bighorn sheep (Ovis canadensis ; Hogg, Forbes, Steele, & Luikart, 2006), Scandanavian gray wolves (Åkesson et al., 2016), and Tasmanian devil (McLennan, Grueber, Wise, Belov, & Hogg, 2020). From these examples, pedigrees have continued to provide an invaluable resource for understanding and managing diversity in plants and animals. However, there are pitfalls for pedigrees that can affect their accuracy and utility for conservation efforts.