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.