Limits...
Next-generation museomics disentangles one of the largest primate radiations.

Guschanski K, Krause J, Sawyer S, Valente LM, Bailey S, Finstermeier K, Sabin R, Gilissen E, Sonet G, Nagy ZT, Lenglet G, Mayer F, Savolainen V - Syst. Biol. (2013)

Bottom Line: We conclude that the extraordinary radiation of guenons has been a complex process driven by, among other factors, localized fluctuations of African forest cover.We find incongruences between phylogenetic trees reconstructed from mitochondrial and nuclear DNA sequences, which can be explained by either incomplete lineage sorting or hybridization.Furthermore, having produced the largest mitochondrial DNA data set from museum specimens, we document how NGS technologies can "unlock" museum collections, thereby helping to unravel the tree-of-life.

View Article: PubMed Central - PubMed

Affiliation: Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot SL5 7PY, UK.

ABSTRACT
Guenons (tribe Cercopithecini) are one of the most diverse groups of primates. They occupy all of sub-Saharan Africa and show great variation in ecology, behavior, and morphology. This variation led to the description of over 60 species and subspecies. Here, using next-generation DNA sequencing (NGS) in combination with targeted DNA capture, we sequenced 92 mitochondrial genomes from museum-preserved specimens as old as 117 years. We infer evolutionary relationships and estimate divergence times of almost all guenon taxa based on mitochondrial genome sequences. Using this phylogenetic framework, we infer divergence dates and reconstruct ancestral geographic ranges. We conclude that the extraordinary radiation of guenons has been a complex process driven by, among other factors, localized fluctuations of African forest cover. We find incongruences between phylogenetic trees reconstructed from mitochondrial and nuclear DNA sequences, which can be explained by either incomplete lineage sorting or hybridization. Furthermore, having produced the largest mitochondrial DNA data set from museum specimens, we document how NGS technologies can "unlock" museum collections, thereby helping to unravel the tree-of-life.

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Related in: MedlinePlus

Ancestral ranges and the timing of diversification in guenons. Only a single representative for each taxon is shown, for the full tree see Figure 2 and Supplementary Figure S3. Pie charts at the nodes indicate ancestral areas, with color corresponding to the location of these areas on the map of Africa shown in the upper left corner. The relative proportion of each color represents the fraction of the global likelihood for the given geographic area. Gray bars indicate the timing of 4 main speciation events (see “Results” section). Vertical bars next to the species names refer to the species groups with photographs showing one of the species group' members (Mi: C. mitis group, C: C. cephus group, P: C. preussi group, Mo: C. mona group, N: C. neglectus group, Di: C. diana group, A: C. aethiops group, D: C. dryas groups, and H: C. hamlyni group). Tip labels in red highlight the members of the terrestrial clade, also see legend of Figure 2. Myr = million years. Ancestral ranges: A, Congo basin; B, northern DRC; C, northern Rift Valley; D, Upper Guinea; G, Lower Guinea; I, Angola; J, southeastern DRC; K, southeastern Africa; L, northeastern Africa; M, Zambia; N, Ethiopia/Sudan. Photograph of C. m. albogularis by Y.A. de Jong and T.M. Butynski—wildsolutions.nl.
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Figure 1: Ancestral ranges and the timing of diversification in guenons. Only a single representative for each taxon is shown, for the full tree see Figure 2 and Supplementary Figure S3. Pie charts at the nodes indicate ancestral areas, with color corresponding to the location of these areas on the map of Africa shown in the upper left corner. The relative proportion of each color represents the fraction of the global likelihood for the given geographic area. Gray bars indicate the timing of 4 main speciation events (see “Results” section). Vertical bars next to the species names refer to the species groups with photographs showing one of the species group' members (Mi: C. mitis group, C: C. cephus group, P: C. preussi group, Mo: C. mona group, N: C. neglectus group, Di: C. diana group, A: C. aethiops group, D: C. dryas groups, and H: C. hamlyni group). Tip labels in red highlight the members of the terrestrial clade, also see legend of Figure 2. Myr = million years. Ancestral ranges: A, Congo basin; B, northern DRC; C, northern Rift Valley; D, Upper Guinea; G, Lower Guinea; I, Angola; J, southeastern DRC; K, southeastern Africa; L, northeastern Africa; M, Zambia; N, Ethiopia/Sudan. Photograph of C. m. albogularis by Y.A. de Jong and T.M. Butynski—wildsolutions.nl.

Mentions: A number of factors might have contributed to the evolutionary radiation of guenons. Guenons occupy a wide geographic range, being distributed over most of sub-Saharan Africa (Butynski 2003). Since the majority of guenons are forest-dwellers, the evolution of new species may have been driven by isolation in forest refugia. Guenon speciation is thought to have taken place during the last 10 myr (Disotell and Raaum 2003), a time period marked by major climatic changes in tropical Africa (Bonnefille 2010). It is thus possible that repeated geographic isolation, leading to reduced gene flow between populations, resulted in the diversity of taxa seen today (i.e., allopatric speciation). Guenons are well known for their morphological (Fig. 1) and acoustic diversity (Kingdon 1980, 1988; Gautier 1988)—traits that can be subject to mate choice. The evolution of these characteristics together with differences in behavior is hypothesized to contribute to species recognition. Furthermore, guenons exhibit a great cytogenetic diversity, with diploid chromosome numbers ranging from 48 to 72 (Dutrillaux et al. 1988; Moulin et al. 2008), which may convey reproductive isolation. Finally, hybridization could have been involved in the evolution of guenons, as documented in other mammals (Arnold and Meyer 2006; Larsen et al. 2010). Interspecies mating in guenons is well known from captivity and the wild and is reported to produce viable and fertile offspring (Detwiler et al. 2005). Furthermore, many extant guenon taxa occur in sympatry and frequently form polyspecific troops (Gautier-Hion 1988), which allows for interspecific or even intergeneric hybridization.


Next-generation museomics disentangles one of the largest primate radiations.

Guschanski K, Krause J, Sawyer S, Valente LM, Bailey S, Finstermeier K, Sabin R, Gilissen E, Sonet G, Nagy ZT, Lenglet G, Mayer F, Savolainen V - Syst. Biol. (2013)

Ancestral ranges and the timing of diversification in guenons. Only a single representative for each taxon is shown, for the full tree see Figure 2 and Supplementary Figure S3. Pie charts at the nodes indicate ancestral areas, with color corresponding to the location of these areas on the map of Africa shown in the upper left corner. The relative proportion of each color represents the fraction of the global likelihood for the given geographic area. Gray bars indicate the timing of 4 main speciation events (see “Results” section). Vertical bars next to the species names refer to the species groups with photographs showing one of the species group' members (Mi: C. mitis group, C: C. cephus group, P: C. preussi group, Mo: C. mona group, N: C. neglectus group, Di: C. diana group, A: C. aethiops group, D: C. dryas groups, and H: C. hamlyni group). Tip labels in red highlight the members of the terrestrial clade, also see legend of Figure 2. Myr = million years. Ancestral ranges: A, Congo basin; B, northern DRC; C, northern Rift Valley; D, Upper Guinea; G, Lower Guinea; I, Angola; J, southeastern DRC; K, southeastern Africa; L, northeastern Africa; M, Zambia; N, Ethiopia/Sudan. Photograph of C. m. albogularis by Y.A. de Jong and T.M. Butynski—wildsolutions.nl.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3676678&req=5

Figure 1: Ancestral ranges and the timing of diversification in guenons. Only a single representative for each taxon is shown, for the full tree see Figure 2 and Supplementary Figure S3. Pie charts at the nodes indicate ancestral areas, with color corresponding to the location of these areas on the map of Africa shown in the upper left corner. The relative proportion of each color represents the fraction of the global likelihood for the given geographic area. Gray bars indicate the timing of 4 main speciation events (see “Results” section). Vertical bars next to the species names refer to the species groups with photographs showing one of the species group' members (Mi: C. mitis group, C: C. cephus group, P: C. preussi group, Mo: C. mona group, N: C. neglectus group, Di: C. diana group, A: C. aethiops group, D: C. dryas groups, and H: C. hamlyni group). Tip labels in red highlight the members of the terrestrial clade, also see legend of Figure 2. Myr = million years. Ancestral ranges: A, Congo basin; B, northern DRC; C, northern Rift Valley; D, Upper Guinea; G, Lower Guinea; I, Angola; J, southeastern DRC; K, southeastern Africa; L, northeastern Africa; M, Zambia; N, Ethiopia/Sudan. Photograph of C. m. albogularis by Y.A. de Jong and T.M. Butynski—wildsolutions.nl.
Mentions: A number of factors might have contributed to the evolutionary radiation of guenons. Guenons occupy a wide geographic range, being distributed over most of sub-Saharan Africa (Butynski 2003). Since the majority of guenons are forest-dwellers, the evolution of new species may have been driven by isolation in forest refugia. Guenon speciation is thought to have taken place during the last 10 myr (Disotell and Raaum 2003), a time period marked by major climatic changes in tropical Africa (Bonnefille 2010). It is thus possible that repeated geographic isolation, leading to reduced gene flow between populations, resulted in the diversity of taxa seen today (i.e., allopatric speciation). Guenons are well known for their morphological (Fig. 1) and acoustic diversity (Kingdon 1980, 1988; Gautier 1988)—traits that can be subject to mate choice. The evolution of these characteristics together with differences in behavior is hypothesized to contribute to species recognition. Furthermore, guenons exhibit a great cytogenetic diversity, with diploid chromosome numbers ranging from 48 to 72 (Dutrillaux et al. 1988; Moulin et al. 2008), which may convey reproductive isolation. Finally, hybridization could have been involved in the evolution of guenons, as documented in other mammals (Arnold and Meyer 2006; Larsen et al. 2010). Interspecies mating in guenons is well known from captivity and the wild and is reported to produce viable and fertile offspring (Detwiler et al. 2005). Furthermore, many extant guenon taxa occur in sympatry and frequently form polyspecific troops (Gautier-Hion 1988), which allows for interspecific or even intergeneric hybridization.

Bottom Line: We conclude that the extraordinary radiation of guenons has been a complex process driven by, among other factors, localized fluctuations of African forest cover.We find incongruences between phylogenetic trees reconstructed from mitochondrial and nuclear DNA sequences, which can be explained by either incomplete lineage sorting or hybridization.Furthermore, having produced the largest mitochondrial DNA data set from museum specimens, we document how NGS technologies can "unlock" museum collections, thereby helping to unravel the tree-of-life.

View Article: PubMed Central - PubMed

Affiliation: Imperial College London, Silwood Park Campus, Buckhurst Road, Ascot SL5 7PY, UK.

ABSTRACT
Guenons (tribe Cercopithecini) are one of the most diverse groups of primates. They occupy all of sub-Saharan Africa and show great variation in ecology, behavior, and morphology. This variation led to the description of over 60 species and subspecies. Here, using next-generation DNA sequencing (NGS) in combination with targeted DNA capture, we sequenced 92 mitochondrial genomes from museum-preserved specimens as old as 117 years. We infer evolutionary relationships and estimate divergence times of almost all guenon taxa based on mitochondrial genome sequences. Using this phylogenetic framework, we infer divergence dates and reconstruct ancestral geographic ranges. We conclude that the extraordinary radiation of guenons has been a complex process driven by, among other factors, localized fluctuations of African forest cover. We find incongruences between phylogenetic trees reconstructed from mitochondrial and nuclear DNA sequences, which can be explained by either incomplete lineage sorting or hybridization. Furthermore, having produced the largest mitochondrial DNA data set from museum specimens, we document how NGS technologies can "unlock" museum collections, thereby helping to unravel the tree-of-life.

Show MeSH
Related in: MedlinePlus