4.2 | Conservation unit designations in the light of complex demographic histories
Given current rates of extirpation and extinction, it is imperative to have strong, scientifically supported management frameworks, particularly given tight resources for conservation (Jackiw, Mandil, & Hager, 2015). Recent work shows that admixture between lineages is common (Coates et al., 2018; vonHoldt et al., 2017), and that new sequencing technologies are allowing us to uncover the complex demographic histories of threatened taxa (Supple & Shapiro, 2018; vonHoldt et al., 2017). Both for caribou and more broadly, now is the time to decide what this means for management and conservation unit designations.
Recent discussion has highlighted that ‘hybrid’ level gene flow is not always negative, particularly in inbred populations or those needing to adapt to rapid change where admixture could be an important source of variation (Supple & Shapiro, 2018, vonHoldt et al., 2017). For example, we find the barrenground caribou to be very admixed and also to have the lowest individual inbreeding co-efficients, and similarly eastern migratory caribou from Ontario/Manitoba have lower inbreeding co-efficients than the non-admixed individuals from Quebec/Labrador (Table S1). Some argue that gene flow could even be facilitated to aid populations under threat from climate change (i.e. genetic rescue; Hamilton & Miller, 2015), which would be easiest between intra-specific populations (Hedrick & Fredrickson, 2010). Good conservation unit designations with an understanding of natural patterns of admixture is key to assess the potential to use such a strategy (Coates et al., 2018). Most discussions have focussed on policy for inter-species hybridisation (but see Coates et al., 2018; Supple & Shapiro, 2018), but a clear framework for conservation unit designation of admixed intra-specific lineages is needed.
Conservation unit designations depend on the goal of conservation, and whether the focus is on the preservation of phenotypes (or ‘pure’ genomes), or evolutionary and ecological processes to maintain resilience of an ecosystem (Fitzpatrick et al., 2015; vonHoldt et al.. 2017; Waples & Lindley, 2018). The latter is likely more useful when attempting to designate units for non-discreet entities, such as we see in caribou. With this in mind, some authors have suggested a flexible approach with each case considered on a context specific basis (Jakiw et al., 2015), whereas others promote the need for a structured and uniform framework to decide on management decisions (Coates et al., 2018). For caribou, it seems appropriate for a structured approach in the naming of subspecies. Coates et al., (2018) suggest that subspecies show local adaptation with or without gene flow. Coupling this idea with our phylogenomic and population genomic results and results from previous studies, Canadian caribou appear to fit into three subspecies; those in the NAL, those in the BEL, and Peary caribou which sit phylogenetically in the BEL but show strong population genomic differences and clear local adaptation of phenotype (Banfield, 1961; COSEWIC, 2011).
The most relevant application of our findings is in the delineation of conservation units in a species with complex and admixed evolutionary histories. We recommend that previously defined Designatable Units based on subspecies and subspecific ecotypes be reconsidered: specifically, because the boreal caribou from the Northwest Territories sit within a different lineage to the other caribou within the boreal DU and appear to have evolved in parallel, they could be split into separate DUs. Further fine scale work will be needed to refine the boundary of the BEL boreal vs the NAL boreal DU. Similarly, given the apparent parallel evolution of the eastern migratory ecotype and the different levels of admixture of Ontario/Manitoba vs Quebec/Labrador populations with the BEL lineage, should be divided into separate DUs. Consideration of whether this will help maximise the resilience of the ecosystem is needed, but this would match the evolutionary processes which have led to the evolution of the groups. Confusingly, Grant’s caribou and barrenground caribou are currently separate subspecies but one DU. Barrenground caribou are very admixed which contrasts with the Grant’s caribou we sampled and so perhaps they warrant listing as separate DUs. Further sampling is needed to resolve the mountain caribou, especially the central mountain population which has been shown to have mitochondrial DNA from both the BEL and NAL lineages (McDevitt et al., 2009). Additionally, genomic data from the southern mountain, and all other DUs not included in this study, is needed to further resolve the complex evolutionary histories and patterns of introgression more broadly. These divisions have significant implications for the status listing of each DU as threat status is assessed based on criteria such as abundance, and priority for management is given to DUs at greatest risk of extinction (COSEWIC, 2015). Given recent rapid declines in both range and population sizes, efficient conservation strategies are needed for caribou.
Our guidelines add to the current discussion about management of admixed populations and those with complex demographic histories (Coates et al., 2018; Fitzpatrick et al., 2015; Hamilton & Miller, 2015; Jackiw et al., 2015; Supple & Shapiro, 2018; vonHoldt et al., 2017). Namely, that subspecies designations are useful and could follow a structured framework (Coates et al., 2018), but that conservation units below the subspecies level likely require a case by case consideration especially given different regulations in different countries (Coates et al., 2018, vonHoldt et al., 2017). Many taxa are facing an increasing threat from climate change and habitat destruction (Hoffman et al., 2017; Ikeda et al., 2017) and genomic data and appropriate conservation unit designations will help with prioritisation given limited resources. Further, genomic data are essential for decisions of genetic rescue strategies. A key next step to achieve these goals, including for caribou, is to investigate adaptive genomic variation to incorporate with demographic history information (Funk, McKay, Hohenloe, & Allendorf, 2012; Funk, Forester, Converse, Darst, & Moreys, 2019).