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

Antunes A, Troyer JL, Roelke ME, Pecon-Slattery J, Packer C, Winterbach C, Winterbach H, Hemson G, Frank L, Stander P, Siefert L, Driciru M, Funston PJ, Alexander KA, Prager KC, Mills G, Wildt D, Bush M, O'Brien SJ, Johnson WE - PLoS Genet. (2008)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Genomic Diversity, National Cancer Institute, Frederick, Maryland, United States of America.

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.

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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 FIVPle pol-RT sequences. The distinct FIVPle 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 FIVPle pol-RT sequence for a representative subset of individuals. (C) Distinctiveness of host and viral molecular genetics in lion populations.
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pgen-1000251-g004: 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 FIVPle pol-RT sequences. The distinct FIVPle 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 FIVPle pol-RT sequence for a representative subset of individuals. (C) Distinctiveness of host and viral molecular genetics in lion populations.

Mentions: These contrasting nDNA and mtDNA results may be indicative of differences in dispersal patterns between males and females, which would be consistent with evidence that females are more phylopatric than males. Alternatively, selection for matrilineally transmitted traits upon which neutral mtDNA alleles hitchhike is possible, given the low values of nucleotide diversity of the mtDNA (π = 0.0066). A similar process has been suggested in whales (π = 0.0007) [25] and African savannah elephants (π = 0.0200) [26], where both species have female phylopatry and like lions, a matriarchal social structure. However, genetic drift tends to overwhelm selection in small isolated populations, predominantly affecting haploid elements due to its lower effective population size (Table 1). Therefore, we suggest that the contrasting results obtained for nDNA and mtDNA are more likely further evidence that lion populations underwent severe bottlenecks. The highly structured lion matrilines comprise four monophyletic mtDNA haplo-groups (Figure 4A; Figure S3). Lineage I consisted of a divergent haplotype H4 from Ken, lineage II was observed in most Southern Africa populations, lineage III was widely distributed from Central and Northern Africa to Asia, and lineage IV occurred in Southern and Eastern Africa.


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

Antunes A, Troyer JL, Roelke ME, Pecon-Slattery J, Packer C, Winterbach C, Winterbach H, Hemson G, Frank L, Stander P, Siefert L, Driciru M, Funston PJ, Alexander KA, Prager KC, Mills G, Wildt D, Bush M, O'Brien SJ, Johnson WE - PLoS Genet. (2008)

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 FIVPle pol-RT sequences. The distinct FIVPle 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 FIVPle pol-RT sequence for a representative subset of individuals. (C) Distinctiveness of host and viral molecular genetics in lion populations.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2572142&req=5

pgen-1000251-g004: 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 FIVPle pol-RT sequences. The distinct FIVPle 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 FIVPle pol-RT sequence for a representative subset of individuals. (C) Distinctiveness of host and viral molecular genetics in lion populations.
Mentions: These contrasting nDNA and mtDNA results may be indicative of differences in dispersal patterns between males and females, which would be consistent with evidence that females are more phylopatric than males. Alternatively, selection for matrilineally transmitted traits upon which neutral mtDNA alleles hitchhike is possible, given the low values of nucleotide diversity of the mtDNA (π = 0.0066). A similar process has been suggested in whales (π = 0.0007) [25] and African savannah elephants (π = 0.0200) [26], where both species have female phylopatry and like lions, a matriarchal social structure. However, genetic drift tends to overwhelm selection in small isolated populations, predominantly affecting haploid elements due to its lower effective population size (Table 1). Therefore, we suggest that the contrasting results obtained for nDNA and mtDNA are more likely further evidence that lion populations underwent severe bottlenecks. The highly structured lion matrilines comprise four monophyletic mtDNA haplo-groups (Figure 4A; Figure S3). Lineage I consisted of a divergent haplotype H4 from Ken, lineage II was observed in most Southern Africa populations, lineage III was widely distributed from Central and Northern Africa to Asia, and lineage IV occurred in Southern and Eastern Africa.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Genomic Diversity, National Cancer Institute, Frederick, Maryland, United States of America.

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.

Show MeSH
Related in: MedlinePlus