The influence of the arid Andean high plateau on the phylogeography and population genetics of guanaco (Lama guanicoe) in South America

Abstract

A comprehensive study of the phylogeography and population genetics of the largest wild artiodactyl in the arid and cold-temperate South American environments, the guanaco (Lama guanicoe) was conducted. Patterns of molecular genetic structure were described using 514 bp of mtDNA sequence and 14 biparentally inherited microsatellite markers from 314 samples. These individuals originated from 17 localities throughout the current distribution across Peru, Bolivia, Argentina and Chile. This confirmed well-defined genetic differentiation and subspecies designation of populations geographically separated to the northwest (L. g. cacsilensis) and southeast (L. g. guanicoe) of the central Andes plateau. However, these populations are not completely isolated, as shown by admixture prevalent throughout a limited contact zone, and a strong signal of expansion from north to south in the beginning of the Holocene. Microsatellite analyses differentiated three northwestern and 4-5 southeastern populations, suggesting patterns of genetic contact among these populations. Possible genetic refuges were identified, as were source-sink patterns of gene flow at historical and recent time scales. Conservation and management of guanaco should be implemented with an understanding of these local population dynamics while also considering the preservation of broader adaptive variation and evolutionary processes.

Fig. 1

Geographic distribution of Lama guanicoe in South America (in dark-grey based on González et al. 2006) showing genetic divisions by subspecies determined by mitochondrial BAPS (red and green continuous lines) and STRUCTURE K=2 (red and green-backed line) analyses, contact zone (yellow line) obtained by microsatellite assignations (STRUCTURE, see Table 3), and populations (blue lines) identified by microsatellite BAPS (1A). Gene flow among populations identified by microsatellite BAPS analyses. The thickness of the arrow indicates the magnitude of gene flow (1B).

Fig. 2

Support for defining of the number of guanaco population based on the microsatellite data set. (A) Mean L(K) ± SD over 20 runs as a function of K. (B) ΔK (Delta K = mean(|L’’(K)|) /sd(L(K))) following Evanno et al (2005) as a function of K.

Fig. 3

Plot of posterior probability of assignment for 319 guanacos (vertical lines) to two genetic clusters based on Bayesian analysis of variation at 14 microsatellite loci. Individuals are grouped by locality, and localities are indicated along the horizontal axis. Light grey = Genetic Cluster 1: Northwest group; dark grey = Genetic Cluster 2: Southeast group. The tables contain the locations, in light grey and dark grey, show the 7 clusters obtained from STRUCTURE analyses (citation). The numbers in the tables indicates BAPS grouping for comparisons; where i: Hyper-Arid Peru, ii: Chilean Pre-altiplano; iii: Arid Chile and Chilean Peri-Puna, iv: Bolivian Chaco, v: Northern and central Patagonia, vi: Western Patagonia, vii: Southern Patagonia, and viii: Fuegian zone.

Fig. 4

Minimum spanning network representing the relationships among 35 control region haplotypes (see Table 5). Circle sizes correspond to haplotype frequencies.

Fig. 5

Mismatch distribution of pairwise nucleotide differences among control region sequences of northwestern guanacos (A), and southeastern guanacos (B). Gray histograms represent the observed differences and the thin lines represent the ideal distribution as predicted by the model.

Fig 6

(A) Plot of prior (black) and posterior (gray) distributions of Northwest effective population sizes, (B) Southeast and (C) ancestral of Lama guanicoe. (D) Prior (black) and posterior (gray) distributions of divergence time (in years) between Northwest and Southeast clusters. (E) Northwest to Southeast migration rates and (F) Southeast to Northwest migration rates.