History of Diversification and Adaptation from North to South Revealed by Genomic Data: Guanacos from the Desert to Sub-Antarctica

Abstract

The increased availability of quality genomic data has greatly improved the scope and resolution of our understanding of the recent evolutionary history of wild species adapted to extreme environments and their susceptibility to anthropogenic impacts. The guanaco (Lama guanicoe), the largest wild ungulate in South America, is a good example. The guanaco is well adapted to a wide range of habitats, including the Sechura Desert, the high Andes Mountains to the north, and the extreme temperatures and conditions of Navarino Island to the south. Guanacos also have a long history of overexploitation by humans. To assess the evolutionary impact of these challenging habitats on the genomic diversity, we analyzed 38 genomes (∼10 to 16×) throughout their extensive latitudinal distribution from the Sechura and Atacama Desert to southward into Tierra del Fuego Island. These included analyses of patterns of unique differentiation in the north and geographic region further south with admixture among L. g. cacsilensis and L. g. guanicoe. Our findings provide new insights on the divergence of the subspecies ∼800,000 yr BP and document two divergent demographic trajectories and to the initial expansion of guanaco into the more southern portions of the Atacama Desert. Patagonian guanacos have experienced contemporary reductions in effective population sizes, likely the consequence of anthropogenic impacts. The lowest levels of genetic diversity corresponded to their northern and western limits of distribution and some varying degrees of genetic differentiation. Adaptive genomic diversity was strongly linked with environmental variables and was linked with colonization toward the south followed by adaptation.

Keywords: Atacama Desert; Patagonia; camelids; extreme environment; population genomics.

Fig. 1.

The distribution of guanacos resulting largely from genetic isolation among populations. a) A map outlining current L. g. cacsilensis and L. g. guanicoe distributions are highlighted in purple and green, respectively, along with sampled location and in colors that distinguish genetic groups (NW, northwest; MW, midwest; SE, southeast; CP, central Patagonia; WP, western Patagonia; SP, south Patagonia; FZ, Fuegian zone) identified in the phylogeny (d) and PCA (Fig. 2a). b) Nucleotide diversity and Watterson's theta of whole genomes, percentage of heterozygosity and nucleotide diversity, and the graph Tajima's D of each genetic group inserted. c) Graph of private alleles. d) Maximum likelihood topology generated with 1394 UCEs.

Fig. 2.

The structure of guanacos is primarily the result of the genetic isolation of natural populations. a) PCA including the sample set. b) PCA of southern guanaco. c) Nei's genetic distance matrix. d) Genetic ancestry proportion for individuals using ADMIXTURE for each of the K = 4 inferred ancestral populations. e) Spatial genomic structure analysis. Gene flow corridors are shown in blue and putative barriers in orange. f) TreeMix unrooted ML tree of guanaco populations with five migration edges (arrows).

Fig. 3.

Coalescent-based inference of the demographic history of the guanaco population. a) PSMC showing two different main trajectories L. g. cacsilensis and L. g. guanicoe guanaco subspecies, purple for L. g. cacsilensis from NW and green for L. g. guanicoe from SP. b) Stairway Plot of Lama g. guanicoe from CP, WP, SP, and FZ.

Fig. 4.

Analysis of SNPs under adaptive and neutral evolution from the guanaco metapopulation. Three significant RDA axes (P < 0.05) from the guanaco metapopulation adaptive data (a, b) and neutral data (c, d). This visualization encompasses colored circles that represent samples from the different population (colored circles), each potentially indicating traits or groupings, and black arrows denote signify environmental variables. RDAs provide a thorough understanding of the relationships among genomic markers, individual characteristics, and environmental influences among subspecies and across the guanaco population.