Pedigree pitfalls and solutions
One common assumption of pedigrees is that the founding individuals (hereafter, founders) are equally unrelated. As many threatened populations have experienced significant declines before populations are pedigreed, founders from these populations may include more variance in kinship amongst one another than individuals randomly sampled from non-threatened populations. For instance, a study of microsatellite-based relatedness in kākāpō (Strigops habroptilus ) demonstrated that full-sibling and half-sibling relationships were represented amongst founders (Bergner, Jamieson, & Robertson, 2014), which has been confirmed with thousands of genome-wide SNPs (Department of Conservation, unpublished data ). Research in Tasmanian devil has further shown that inferring estimates of relatedness amongst founders using molecular genetic and geographic data reveals significantly higher inbreeding coefficients in the years following establishment, compared to pedigrees that treat founders as equally unrelated (Hogg et al., 2019). While these effects are ameliorated with higher pedigree depth from founding individuals (Balloux et al., 2004), this assumption can be perpetuated when individuals of unknown ancestry (e.g., supplemented individuals, or individuals with missing information) are incorporated into the pedigree in later generations. In addition to these issues, pedigrees are also susceptible to human transcription errors, which can compound in pedigrees over time (Hammerly, de la Cerda, Bailey, & Johnson, 2016).
Missing information is often a concern for wild pedigrees where parentage is difficult to ascertain. For example, accurate parentage can be challenging due to the time and cost required to monitor breeding individuals in the wild, coupled with the breeding behaviour of the organism (e.g., polygamous species like flock breeding birds, herd-breeding mammals, and open-pollinated plants; Ashley, 2010; Ivy, Putnam, Navarro, Gurr, & Ryder, 2016; Wildt et al., 2019). This challenge is exacerbated when individuals lose their identifiers (e.g., radio collars, tags, or leg bands; Milligan, Davis, & Altizer, 2003) or when socially monogamous individuals participate in extra-pair parentage (e.g., Overbeek et al., 2020). Even in captivity, parentage amongst polygynous breeders is difficult to track. Individuals with unknown parentage are either excluded from the potential breeding population due to kinship uncertainty, are assigned a multiple parentage average kinship value (i.e., MULTs; Lacy, 2012), or are assigned hypothetical parentage which reconstructs an assumed pedigree (Ballou et al., 2010). Building MULTs into a pedigree has been shown to retain greater genetic diversity while still maintaining inbreeding avoidance as opposed to removing individuals of unknown parentage, as shown in Arabian oryx (Oryx leucoryx ; Putnam & Ivy, 2014). However, for species that experience large differences in reproductive success between individuals, the MULT approach has been shown to both over- and under-estimate individual genetic contributions (e.g., Tasmanian devil; Farquharson, Hogg, & Grueber, 2019). To highlight the severity of such challenges in group breeding species, over 50% of ungulate species managed under the auspices of the Association of Zoos and Aquariums Species Survival Plan® (SSP) have less than half of their pedigree known; in fact, only 15% have completely known pedigrees (R.M.Gooley and E.K.Latch, unpublished data ). This is a common challenge encountered with group-housed captive populations, which can lead to management challenges with respect to kinship calculations, breeding recommendations, and genetic diversity retention (Hauser, Galla, Steeves, & Latch, Preprint ). Resolving unknown parentage and generating accurate kinship values would lead to more effective conservation management of intensively managed wild and captive populations.
To address pedigree challenges, empirical estimates of relatedness from DNA and geographic data can be used to complete and complement pedigrees. 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 maintain use, 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 (Taylor 2015; Flanagan et al., 2019; Galla et al., 2020). Empirical data have been used to enhance pedigrees for use in conservation management, including estimating founder relationships (Hogg et al., 2019) and reconstructing pedigrees (Gooley, Hogg, Belov, & Grueber, 2017; McLennan et al., 2018) in Tasmanian devils and guiding metapopulation management of pedigreed and non-pedigreed populations of sable antelope (Hippotragus niger ) and dama gazelle (Nanger dama ; R.M.Gooley Personal comm. ). Molecular data can also be used to validate uncertain and semi-wild pedigrees. For example, microsatellite markers have recently been used to validate pedigrees for intensively-monitored and critically endangered wild populations of kakī/black stilt (Himantopus novaezelandiae ; Overbeek et al., 2020) and black robin (Petroica traversi; Forsdick, Cubrinovska, Massaro, & Hale, 2021).
Fellow conservation practitioners and researchers have queried whether time and resources should be dedicated towards building pedigrees from scratch and maintaining them, considering their caveats and the abundance of HTS data available to produce estimates of relatedness that are comparable to pedigrees (Speed & Balding, 2015). In this perspective, we argue that pedigrees remain an invaluable tool in the conservation genomics era, providing an affordable way to estimate relatedness and inbreeding (Nietlisbach et al., 2017, but see also Kardos, Luikart, & Allendorf, 2015), enhance genomic inquiry, and capture important metadata that genomic data alone cannot (Fig. 1). Based on our collective experience, we assert that gathering the behavioural and ecological data that underlie pedigrees not only advances our understanding of inter-individual relationships, but also develops strong ties between conservation geneticists, practitioners, and beyond (see below). In the conservation genomics era, we posit that the greatest conservation genomic advances will happen when we invest in both pedigree and genomic data.