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Genetic diversity and population history of a critically endangered primate, the northern muriqui (Brachyteles hypoxanthus).

Chaves PB, Alvarenga CS, Possamai Cde B, Dias LG, Boubli JP, Strier KB, Mendes SL, Fagundes V - PLoS ONE (2011)

Bottom Line: We analyzed the mitochondrial DNA control region of 152 northern muriquis, or 17.6% of the 864 northern muriquis from 8 of the 12 known extant populations and found no evidence of phylogeographic partitions or past population shrinkage/expansion.In addition, the best scenario supported by an Approximate Bayesian Computation analysis, significant fixation indices (Φ(ST) = 0.49, Φ(CT) = 0.24), and population-specific haplotypes, coupled with the extirpation of intermediate populations, are indicative of a recent geographic structuring of genetic diversity during the Holocene.We suggest that these populations be treated as discrete units for conservation management purposes.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Ciências Biológicas, Universidade Federal do Espírito Santo, Vitória, Espírito Santo, Brazil.

ABSTRACT
Social, ecological, and historical processes affect the genetic structure of primate populations, and therefore have key implications for the conservation of endangered species. The northern muriqui (Brachyteles hypoxanthus) is a critically endangered New World monkey and a flagship species for the conservation of the Atlantic Forest hotspot. Yet, like other neotropical primates, little is known about its population history and the genetic structure of remnant populations. We analyzed the mitochondrial DNA control region of 152 northern muriquis, or 17.6% of the 864 northern muriquis from 8 of the 12 known extant populations and found no evidence of phylogeographic partitions or past population shrinkage/expansion. Bayesian and classic analyses show that this finding may be attributed to the joint contribution of female-biased dispersal, demographic stability, and a relatively large historic population size. Past population stability is consistent with a central Atlantic Forest Pleistocene refuge. In addition, the best scenario supported by an Approximate Bayesian Computation analysis, significant fixation indices (Φ(ST) = 0.49, Φ(CT) = 0.24), and population-specific haplotypes, coupled with the extirpation of intermediate populations, are indicative of a recent geographic structuring of genetic diversity during the Holocene. Genetic diversity is higher in populations living in larger areas (>2,000 hectares), but it is remarkably low in the species overall (θ = 0.018). Three populations occurring in protected reserves and one fragmented population inhabiting private lands harbor 22 out of 23 haplotypes, most of which are population-exclusive, and therefore represent patchy repositories of the species' genetic diversity. We suggest that these populations be treated as discrete units for conservation management purposes.

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Nine alternative scenarios tested with the Approximates Bayesian Computation approach.Only the four best sampled populations were included (PESB, PERD, RPPN-FMA, and SMJ). The scenarios are organized in three groups of three each. The first group includes scenarios that depicts a rapid or star-like divergence event among the populations (1, 2, and 3). Scenario 1 assumes that one large population split into four populations during the Holocene (t1). Scenarios 2 and 3 push the splitting event further back in time (during the last glacial maximum, t2, and earlier, t3, respectively). The second group includes three scenarios (3, 4, and 5) representing sequential or step-wise divergence among the populations in different times. The third group includes scenarios with sequential divergences and assumes that the population RPPN-FMA (FMA) diverged after an admixture event. Different branch colors represent putative changes in effective population sizes (see Figure S1 for prior set up). The posterior probability of each scenario is shown on the lower left-hand side of its respective diagram.
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pone-0020722-g002: Nine alternative scenarios tested with the Approximates Bayesian Computation approach.Only the four best sampled populations were included (PESB, PERD, RPPN-FMA, and SMJ). The scenarios are organized in three groups of three each. The first group includes scenarios that depicts a rapid or star-like divergence event among the populations (1, 2, and 3). Scenario 1 assumes that one large population split into four populations during the Holocene (t1). Scenarios 2 and 3 push the splitting event further back in time (during the last glacial maximum, t2, and earlier, t3, respectively). The second group includes three scenarios (3, 4, and 5) representing sequential or step-wise divergence among the populations in different times. The third group includes scenarios with sequential divergences and assumes that the population RPPN-FMA (FMA) diverged after an admixture event. Different branch colors represent putative changes in effective population sizes (see Figure S1 for prior set up). The posterior probability of each scenario is shown on the lower left-hand side of its respective diagram.

Mentions: We adopted a four-step approach to infer changes in the population size of northern muriquis. First, we calculated the neutrality tests FS [54], DF and F [55], and R2 [56], in DNASP 5.0 [57]. These tests are suitable for detecting different types of demographic events (i.e. sudden expansion, sudden contraction, and bottleneck) in our data set [58]. Very low and significant results of neutrality tests in mtDNA can be interpreted as evidence for population expansion. Significance was calculated after 50,000 coalescent simulations. Second, we calculated the exponential growth rate (g) in a coalescent framework using the Bayesian module in LAMARC 2.1.3 [59]. One long Markov Chain Monte Carlo (MCMC) run was performed with 2 million generations, sampling every 20th step and a heating scheme of 4 simultaneous chains with different temperatures (1, 1.2, 1.5, and 3). Third, we used BEAST 1.4.8 [60] to estimate the Bayesian skyline plot (BSP) to depict changes in effective population size over time. A normal distribution from the substitution rate estimated for Ateles (see Substitution rate) was used in BEAST. We ran the program for 100 million generations, with a sampling interval of 5,000 generations. Finally, we tested nine alternative scenarios for the diversification of four muriqui populations using the Approximate Bayesian Computation (ABC) approach implemented in DIYABC 1.0.4.38beta [61]. We ran a total of 9 million simulations (1,000,000 per scenario) and used the logistic regression method to calculate the posterior probabilities of each scenario (see Fig. 2 and Figure S1 for details). To minimize computation time and circumvent possible sampling bias that would affect the estimates, all coalescent analyses were carried out with a subset of 106 sequences. This smaller sample size was obtained after drawing 25 random samples from each RPPN-FMA and SMJ. Given the shallow haplotype network and lack of strong monophyletic subgroups (see Results), all samples were treated as a single population in the first three treatments.


Genetic diversity and population history of a critically endangered primate, the northern muriqui (Brachyteles hypoxanthus).

Chaves PB, Alvarenga CS, Possamai Cde B, Dias LG, Boubli JP, Strier KB, Mendes SL, Fagundes V - PLoS ONE (2011)

Nine alternative scenarios tested with the Approximates Bayesian Computation approach.Only the four best sampled populations were included (PESB, PERD, RPPN-FMA, and SMJ). The scenarios are organized in three groups of three each. The first group includes scenarios that depicts a rapid or star-like divergence event among the populations (1, 2, and 3). Scenario 1 assumes that one large population split into four populations during the Holocene (t1). Scenarios 2 and 3 push the splitting event further back in time (during the last glacial maximum, t2, and earlier, t3, respectively). The second group includes three scenarios (3, 4, and 5) representing sequential or step-wise divergence among the populations in different times. The third group includes scenarios with sequential divergences and assumes that the population RPPN-FMA (FMA) diverged after an admixture event. Different branch colors represent putative changes in effective population sizes (see Figure S1 for prior set up). The posterior probability of each scenario is shown on the lower left-hand side of its respective diagram.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3108597&req=5

pone-0020722-g002: Nine alternative scenarios tested with the Approximates Bayesian Computation approach.Only the four best sampled populations were included (PESB, PERD, RPPN-FMA, and SMJ). The scenarios are organized in three groups of three each. The first group includes scenarios that depicts a rapid or star-like divergence event among the populations (1, 2, and 3). Scenario 1 assumes that one large population split into four populations during the Holocene (t1). Scenarios 2 and 3 push the splitting event further back in time (during the last glacial maximum, t2, and earlier, t3, respectively). The second group includes three scenarios (3, 4, and 5) representing sequential or step-wise divergence among the populations in different times. The third group includes scenarios with sequential divergences and assumes that the population RPPN-FMA (FMA) diverged after an admixture event. Different branch colors represent putative changes in effective population sizes (see Figure S1 for prior set up). The posterior probability of each scenario is shown on the lower left-hand side of its respective diagram.
Mentions: We adopted a four-step approach to infer changes in the population size of northern muriquis. First, we calculated the neutrality tests FS [54], DF and F [55], and R2 [56], in DNASP 5.0 [57]. These tests are suitable for detecting different types of demographic events (i.e. sudden expansion, sudden contraction, and bottleneck) in our data set [58]. Very low and significant results of neutrality tests in mtDNA can be interpreted as evidence for population expansion. Significance was calculated after 50,000 coalescent simulations. Second, we calculated the exponential growth rate (g) in a coalescent framework using the Bayesian module in LAMARC 2.1.3 [59]. One long Markov Chain Monte Carlo (MCMC) run was performed with 2 million generations, sampling every 20th step and a heating scheme of 4 simultaneous chains with different temperatures (1, 1.2, 1.5, and 3). Third, we used BEAST 1.4.8 [60] to estimate the Bayesian skyline plot (BSP) to depict changes in effective population size over time. A normal distribution from the substitution rate estimated for Ateles (see Substitution rate) was used in BEAST. We ran the program for 100 million generations, with a sampling interval of 5,000 generations. Finally, we tested nine alternative scenarios for the diversification of four muriqui populations using the Approximate Bayesian Computation (ABC) approach implemented in DIYABC 1.0.4.38beta [61]. We ran a total of 9 million simulations (1,000,000 per scenario) and used the logistic regression method to calculate the posterior probabilities of each scenario (see Fig. 2 and Figure S1 for details). To minimize computation time and circumvent possible sampling bias that would affect the estimates, all coalescent analyses were carried out with a subset of 106 sequences. This smaller sample size was obtained after drawing 25 random samples from each RPPN-FMA and SMJ. Given the shallow haplotype network and lack of strong monophyletic subgroups (see Results), all samples were treated as a single population in the first three treatments.

Bottom Line: We analyzed the mitochondrial DNA control region of 152 northern muriquis, or 17.6% of the 864 northern muriquis from 8 of the 12 known extant populations and found no evidence of phylogeographic partitions or past population shrinkage/expansion.In addition, the best scenario supported by an Approximate Bayesian Computation analysis, significant fixation indices (Φ(ST) = 0.49, Φ(CT) = 0.24), and population-specific haplotypes, coupled with the extirpation of intermediate populations, are indicative of a recent geographic structuring of genetic diversity during the Holocene.We suggest that these populations be treated as discrete units for conservation management purposes.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Ciências Biológicas, Universidade Federal do Espírito Santo, Vitória, Espírito Santo, Brazil.

ABSTRACT
Social, ecological, and historical processes affect the genetic structure of primate populations, and therefore have key implications for the conservation of endangered species. The northern muriqui (Brachyteles hypoxanthus) is a critically endangered New World monkey and a flagship species for the conservation of the Atlantic Forest hotspot. Yet, like other neotropical primates, little is known about its population history and the genetic structure of remnant populations. We analyzed the mitochondrial DNA control region of 152 northern muriquis, or 17.6% of the 864 northern muriquis from 8 of the 12 known extant populations and found no evidence of phylogeographic partitions or past population shrinkage/expansion. Bayesian and classic analyses show that this finding may be attributed to the joint contribution of female-biased dispersal, demographic stability, and a relatively large historic population size. Past population stability is consistent with a central Atlantic Forest Pleistocene refuge. In addition, the best scenario supported by an Approximate Bayesian Computation analysis, significant fixation indices (Φ(ST) = 0.49, Φ(CT) = 0.24), and population-specific haplotypes, coupled with the extirpation of intermediate populations, are indicative of a recent geographic structuring of genetic diversity during the Holocene. Genetic diversity is higher in populations living in larger areas (>2,000 hectares), but it is remarkably low in the species overall (θ = 0.018). Three populations occurring in protected reserves and one fragmented population inhabiting private lands harbor 22 out of 23 haplotypes, most of which are population-exclusive, and therefore represent patchy repositories of the species' genetic diversity. We suggest that these populations be treated as discrete units for conservation management purposes.

Show MeSH
Related in: MedlinePlus