The evolutionary dynamics of the lion Panthera leo revealed by host and viral population genomics

Abstract

The lion Panthera leo is one of the world's most charismatic carnivores and is one of Africa's key predators. Here, we used a large dataset from 357 lions comprehending 1.13 megabases of sequence data and genotypes from 22 microsatellite loci to characterize its recent evolutionary history. Patterns of molecular genetic variation in multiple maternal (mtDNA), paternal (Y-chromosome), and biparental nuclear (nDNA) genetic markers were compared with patterns of sequence and subtype variation of the lion feline immunodeficiency virus (FIV(Ple)), a lentivirus analogous to human immunodeficiency virus (HIV). In spite of the ability of lions to disperse long distances, patterns of lion genetic diversity suggest substantial population subdivision (mtDNA Phi(ST) = 0.92; nDNA F(ST) = 0.18), and reduced gene flow, which, along with large differences in sero-prevalence of six distinct FIV(Ple) subtypes among lion populations, refute the hypothesis that African lions consist of a single panmictic population. Our results suggest that extant lion populations derive from several Pleistocene refugia in East and Southern Africa ( approximately 324,000-169,000 years ago), which expanded during the Late Pleistocene ( approximately 100,000 years ago) into Central and North Africa and into Asia. During the Pleistocene/Holocene transition ( approximately 14,000-7,000 years), another expansion occurred from southern refugia northwards towards East Africa, causing population interbreeding. In particular, lion and FIV(Ple) variation affirms that the large, well-studied lion population occupying the greater Serengeti Ecosystem is derived from three distinct populations that admixed recently.

Figure 1. Geographic location of the lion samples and the variability of host and viral genetic markers among lion populations.

(A) Historical and current geographic distribution of lion, Panthera leo. A three-letter code pointing to a white dotted circle represents the geographic location of the 11 lion populations determined by Bayesian analyses and factorial correspondence analyses of the genetic distinctiveness of 357 lion samples (see text): GIR, Gir Forest, India; UGA, Uganda (Queen Elizabeth National Park); KEN, Kenya (Laikipia), SER, Serengeti National Park, Tanzania; NGC, Ngorongoro Crater, Tanzania; KRU, Kruger National Park, South Africa; BOT-I, southern Botswana and Kalahari, South Africa; BOT-II, northern Botswana; and NAM, Namibia. Green squares represent captive individual samples to explore the relationship of lions from more isolated/endangered/depleted areas: ATL, Morocco Atlas lions (n = 4); ANG, Angola (n = 2); and ZBW, Zimbabwe (n = 1). Deduced historical expansions (M1 and M2) are represented by red arrows (see text). (B) Haplotype frequencies observed in the 11 lion populations for nDNA (ADA and TF), and mtDNA (12S–16S) genes, paralleled with the FIV_Ple serum-prevalence frequencies (black – sero-positive; gray – indeterminate; white – sero-negative). Population sample sizes are indicated within parenthesis. (C) Statistical parsimony networks of lion ADA, TF, and 12S–16S haplotypes. Circle size is proportional to the haplotype frequency and crossbars represent the number of step mutations connecting haplotypes. The mtDNA haplotypes H5 and H6 are shaded gray as they were detected only in the individual samples from ANG, ATL, and ZBW, which do not group in unique population clusters (see text).

Figure 2. Population structure analyses in lions.

(A) Bayesian population assignment test of the 357 lions using 24 nDNA loci (ADA, TF, and 22 microsatellites) and mtDNA data, and considering K = 11 (11 populations). (B) Three-dimensional factorial correspondence analysis (FCA) based on the 24 nDNA loci genotypes in the 357 lions. Axe 1, 2, and 3 represent 49.90% of the genetic variation observed. (C) FCA representation excluding the GIR lions. Axe 1, 2, and 3 represent 51.35% of the genetic variation observed. (D) FCA representation considering only the SER lions supportive of a three distinct population clusters subdivision (SER-I, SER-II, and SER-III).

Figure 3. Genetic differentiation of host and viral genetic markers with geographic distance.

Regression of lion pairwise F _ST (nDNA and mtDNA) and FIV_Ple (pol-RT) on geographic distance.

Figure 4. Evolutionary relationships of the host and viral genetic markers among lion populations.

(A) Unrooted neighbour-joining (NJ) tree from nDNA genotypes of 24 loci (ADA, TF, and 22 microsatellites) in the 11 lion populations (left), and rooted NJ tree for the distinct mtDNA (12S–16S, 1,882 bp) haplotypes in lion (right). The distinct mtDNA lineages were labelled I to IV. Bootstrap support (BPS) values >50 are indicated. (B) NJ tree of the 301 bp FIV_Ple pol-RT sequences. The distinct FIV_Ple subtypes were labelled A to F. BPS values are placed at each branchpoint and in parenthesis are the BPS values obtained for a tree established with 520 bp of FIV_Ple pol-RT sequence for a representative subset of individuals. (C) Distinctiveness of host and viral molecular genetics in lion populations.