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. 2020 Aug;29(15):2793-2809.
doi: 10.1111/mec.15522. Epub 2020 Jul 11.

The role of introgression and ecotypic parallelism in delineating intraspecific conservation units

Rebecca S Taylor  1 , Micheline Manseau  1   2 , Rebekah L Horn  1   3 , Sonesinh Keobouasone  2 , G Brian Golding  4 , Paul J Wilson  1
Affiliations

The role of introgression and ecotypic parallelism in delineating intraspecific conservation units

Rebecca S Taylor et al. Mol Ecol. 2020 Aug.

Abstract

Parallel evolution can occur through selection on novel mutations, standing genetic variation or adaptive introgression. Uncovering parallelism and introgressed populations can complicate management of threatened species as parallelism may have influenced conservation unit designations and admixed populations are not generally considered under legislations. We examined high coverage whole-genome sequences of 30 caribou (Rangifer tarandus) from across North America and Greenland, representing divergent intraspecific lineages, to investigate parallelism and levels of introgression contributing to the formation of ecotypes. Caribou are split into four subspecies and 11 extant conservation units, known as designatable units (DUs), in Canada. Using genomes from all four subspecies and six DUs, we undertake demographic reconstruction and confirm two previously inferred instances of parallel evolution in the woodland subspecies and uncover an additional instance of parallelism of the eastern migratory ecotype. Detailed investigations reveal introgression in the woodland subspecies, with introgressed regions found spread throughout the genomes encompassing both neutral and functional sites. Our investigations using whole genomes highlight the difficulties in unequivocally demonstrating parallelism through adaptive introgression in nonmodel species with complex demographic histories, with standing variation and introgression both potentially involved. Additionally, the impact of parallelism and introgression on conservation policy for management units needs to be considered in general, and the caribou designations will need amending in light of our results. Uncovering and decoupling parallelism and differential patterns of introgression will become prevalent with the availability of comprehensive genomic data from nonmodel species, and we highlight the need to incorporate this into conservation unit designations.

Keywords: adaptive introgression; conservation legislation; demographic history; introgressed populations; management units; parallel evolution.

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Figures

FIGURE 1
FIGURE 1
Range of caribou in North America. Background colours show the ranges of the four subspecies (R. t. caribou; R. t. groenlandicus; R. t. pearyi; R. t. granti). Circles and triangles indicate sampling locations for this study and are coloured by designatable unit. We also included two genomes from Greenland shown by the black circles. A circle indicates that the sample is from the BEL mitochondrial lineage and a triangle means the sample is from the NAL mitochondrial lineage. Sample numbers 1 and 2 are from the Yukon Porcupine herd, 3 and 4 from the Northwest Territories Bluenose herd, 5 and 6 from the Manitoba Qamanirijuaq herd, 7 and 8 from Western Greenland Kangerlussuaq, 9 and 10 from the Northwest Territories Sahtú region, 11 and 12 from the Manitoba Naosap herd, 13 from Ontario Ignace 14 from Ontario Cochrane, 15 and 16 from the Ontario Pen Island herd, 17 and 18 from the Quebec George River herd, 19 and 20 from the Northwest Territories, Redstone herd, 21 and 22 from the British Columbia Atlin herd, 23 and 24 from the British Columbia Frog herd, 25 and 26 from the British Columbia Itcha‐Ilgachuz herd, 27 and 28 from Nunavut Bathurst Island and 29 and 30 from the British Columbia Columbia North herd[Colour figure can be viewed at wileyonlinelibrary.com]
FIGURE 2
FIGURE 2
Principal component analyses of caribou genetic variation. All plots show PC1 (x‐axis) and PC2 (y‐axis) shown by the eigenvalues plot in the corners. The plots show PCA of all 30 caribou and the Inner Mongolian reindeer (a), fine‐scale analysis of the NAL caribou (b), fine‐scale analysis of the BEL caribou, aside from Peary and Western Greenland (c) and fine‐scale analysis of the 14 individuals clustered together from Figure 3c (d)[Colour figure can be viewed at wileyonlinelibrary.com]
FIGURE 3
FIGURE 3
Maximum‐likelihood phylogenomic reconstruction from SNP data in RAxML of 30 caribou and the Inner Mongolian reindeer. We show the unrooted phylogeny for clarity, with the root fixed where indicated in analyses using the Sitka deer as an outgroup (See Figure 5 and Figure S8). Nodes show bootstrap support values[Colour figure can be viewed at wileyonlinelibrary.com]
FIGURE 4
FIGURE 4
Consensus maximum‐likelihood phylogenomic reconstruction from ~4,000 conserved mammalian gene sequences from BUSCO of 30 caribou and the Inner Mongolia reindeer rooted using a Sitka deer outgroup. Nodes show bootstrap support values[Colour figure can be viewed at wileyonlinelibrary.com]
FIGURE 5
FIGURE 5
Reconstruction of effective population size of caribou. Results have been split into two plots given the differences in peak effective population sizes, with (a) showing the NAL lineage and Peary and Western Greenland caribou and (b) showing all other BEL caribou. The effective population sizes remain the same until 100–200 kya where demographic histories start to differ, with peak population sizes 120 kya. NAL caribou have smaller peak effective population sizes than BEL caribou, with Peary and Greenland caribou intermediate[Colour figure can be viewed at wileyonlinelibrary.com]
FIGURE 6
FIGURE 6
Unrooted maximum‐likelihood phylogeny reconstructed in Treemix with no migration events added (a) and an unrooted maximum‐likelihood phylogeny reconstructed in Treemix with 7 migration events added (b) as indicated from the OptM results (Figure S7)[Colour figure can be viewed at wileyonlinelibrary.com]
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