The Evolutionary Dynamics of the Lion Panthera leo Revealed by Host and Viral Population Genomics

Antunes, Agostinho; Troyer, Jennifer L.; Roelke, Melody E.; Pecon-Slattery, Jill; Packer, Craig; Winterbach, Christiaan; Winterbach, Hanlie; Hemson, Graham; Frank, Laurence; Stander, Philip; Siefert, Ludwig; Driciru, Margaret; Funston, Paul J.; Alexander, Kathy A.; Prager, Katherine C.; Mills, Gus; Wildt, David; Bush, Mitch; O'Brien, Stephen J.; Johnson, Warren E.

The lion Panthera leo, a formidable carnivore with a complex cooperative social system, has fascinated humanity since pre-historical times, inspiring hundreds of religious and cultural allusions. Here, we use a comprehensive sample of 357 individuals from most of the major lion populations in Africa and Asia. We assayed appropriately informative autosomal, Y-chromosome, and mitochondrial genetic markers, and assessed the prevalence and genetic variation of the lion-specific feline immunodeficiency virus (FIV Ple ), a lentivirus analogous to human immunodeficiency virus (HIV) that causes AIDS-like immunodeficiency disease in domestic cats. We compare the large multigenic dataset from lions with patterns of genetic variation of the FIV Ple to characterize the population-genomic legacy of lions. We refute the hypothesis that African lions consist of a single panmictic population, highlighting the importance of preserving populations in decline rather than prioritizing larger-scale conservation efforts. Interestingly, lion and FIV Ple variation revealed evidence of unsuspected genetic diversity even in the well-studied lion population of the Serengeti Ecosystem, which consists of recently admixed animals derived from three distinct genetic groups. 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 [22] and factorial correspondence analyses [23] 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). doi:10.1371/journal.pgen.1000251.g001 yield similar inferences of population history, as coalescent times vary as a function of their pattern of inheritance [21] . There is also a large variance in coalescent times across loci sharing a common pattern of inheritance especially in complex demographical histories (Table 1) . However, the accurate interpretation of the differences among loci can provide a more resolved and coherent population history, affording more-nuanced insights on past demographic processes, levels of admixture, taxonomic issues, and on the most appropriate steps for effective conservation