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.