1 | INTRODUCTION
Parallel evolution is a process where divergent populations living in similar environments independently evolve the same or similar traits (Lamichhaney et al., 2017; Oke, Rolshausen, Leblond, & Hendry, 2017). Traditionally, it was assumed that cases of parallelism occurred by either new mutations, or from selection on standing genetic variation (Macpherson & Nuismer, 2017), however, adaptive introgression can also lead to the selection of beneficial alleles (Fraser & Whiting, 2019; Hedrick, 2013; Lee & Coop, 2017). Adaptive introgression between divergent lineages can facilitate parallel evolution, even if traits are controlled by more than one locus. Adaptive introgression could therefore be difficult to distinguish from parallel evolution from standing genetic variation (Bassham, Catchen, Lescak, von Hippel, & Cresko, 2018; Fraser & Whiting, 2019; Hedrick, 2013; Lee & Coop, 2017), and the two may also happen in concert (Bassham et al., 2018; Fraser & Whiting, 2019; Lee & Coop, 2017).
Recent findings show high levels of introgression among taxa (Kumar et al., 2017; Mallet, 2005; Taylor & Larson, 2019), or highly selective introgression of important adaptive genomic regions (e.g. Poelstra et al., 2014; Song et al., 2011; The Heliconius Genome Consortium, 2012). However, admixed or hybrid populations are not generally considered under current conservation legislations (Fitzpatrick, Ryan, Johnson, Corush, & Carter, 2015; vonHoldt, Brzeski, Wilcove, & Rutledge, 2018) and when discussed, the focus is typically on inter-species hybrids and not conservation units below the species level (Fitzpatrick et al., 2015). Given the current extinction crisis under climate change also resulting in range shifts and increased secondary contact (Garroway et al., 2010; Gómez, González-Megías, Lorite, Abdelaziz, & Perfectti, 2015), new management frameworks will be required to encompass more complex evolutionary histories (vonHoldt et al., 2018) and novel adaptive potential.
Here we investigate intra-specific parallelism and levels of introgression contributing to adaptive evolution in the formation of caribou (Rangifer tarandus ) ecotypes across North America and Greenland representing divergent intra-specific lineages. In Canada, there are four caribou subspecies largely based on morphology (Banfield, 1967). Caribou in Canada are distributed in widely different ecozones, including the High Arctic, mountains, taiga, and boreal forests (Banfield, 1967; COSEWIC, 2011). They display evidence of local adaptation, with differences in morphology, diet, behaviour, and life history in different regions, leading to the classification of 12 Designatable Units (DUs; 11 extant and 1 extinct; COSEWIC, 2011; Figure 1 and Figure S1), often referred to as ecotypes, by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC, 2011). Importantly, all 11 extant ecotypes are now listed as at risk of extinction (COSEWIC, 2011-2017) and many have been declining rapidly due to human-mediated disturbances including climate change (Festa-Bianchet, Ray, Boutin, Côté, & Gunn, 2011; Vors & Boyce, 2009; Weckworth, Hebblewhite, Mariani, & Musiani, 2018). Additionally, caribou are of huge cultural, spiritual, and economic significance to many indigenous communities (Festa-Bianchet et al., 2011; Polfus et al., 2016). It is also a keystone species for the ecosystem, important for vegetation structure, nitrogen cycling, and predator populations (Festa-Bianchet et al., 2011).
Previous mitochondrial DNA studies indicate two major phylogenetic lineages of Caribou in North America (Cronin, MacNeil, & Patton, 2005; Flagstad & Røed, 2003; Klütsch, Manseau, & Wilson, 2012; Weckworth, Musiani, Devitt, Hebblewhite, & Mariani, 2012). The range of the boreal DU extends from the east coast of Canada to the northern regions of the Northwest Territories, and in the central and eastern part of the range, the boreal caribou sit within the North American phylogenetic lineage, or NAL (Klütsch et al., 2012; Polfus, Manseau, Klütsch, Simmons, & Wilson, 2017). However, the northern mountain DU and boreal caribou from the northern part of the Northwest Territories belong to the Beringian-Eurasian phylogenetic lineage, or BEL, even though all boreal and northern mountain caribou are currently considered within the woodland subspecies, indicating potential parallel evolution (Polfus et al., 2017). Additionally, the eastern migratory DU has two disjunct ranges, one in northern Manitoba and Ontario and the other in northern Quebec and Labrador (Figure S1). Eastern migratory caribou from the Ontario and Manitoba region were found to be an admixture of boreal caribou from the NAL lineage and barrenground caribou from the BEL lineage (Klütsch, Manseau, Trim, Polfus, & Wilson, 2016). However, it is unknown if the Quebec and Labrador eastern migratory ecotype share the same origin.
We examined high coverage whole-genome sequences of 30 caribou in the most comprehensive study to date covering six DUs and all four subspecies (Figure 1). We used genome-wide variation using population and phylogenomic approaches to investigate instances of parallel evolution. We then elucidated the extent of introgression across the genome among caribou lineages. Issues of parallelism and complex patterns of introgression will certainly become more prevalent and we discuss how the definition and delineation of conservation units could be informed by our results.