Limits...
A six nuclear gene phylogeny of Citrus (Rutaceae) taking into account hybridization and lineage sorting.

Ramadugu C, Pfeil BE, Keremane ML, Lee RF, Maureira-Butler IJ, Roose ML - PLoS ONE (2013)

Bottom Line: We found that 11 of 33 samples appear to be affected by historical hybridization.Analysis of the remaining three genes supported the conclusions from the hybrid detection test.We conclude that identifying hybridization as a frequent cause of incongruence among gene trees is critical to correctly infer the phylogeny among species of Citrus.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Sciences, University of California Riverside, Riverside, California, United States of America.

ABSTRACT

Background: Genus Citrus (Rutaceae) comprises many important cultivated species that generally hybridize easily. Phylogenetic study of a group showing extensive hybridization is challenging. Since the genus Citrus has diverged recently (4-12 Ma), incomplete lineage sorting of ancestral polymorphisms is also likely to cause discrepancies among genes in phylogenetic inferences. Incongruence of gene trees is observed and it is essential to unravel the processes that cause inconsistencies in order to understand the phylogenetic relationships among the species.

Methodology and principal findings: (1) We generated phylogenetic trees using haplotype sequences of six low copy nuclear genes. (2) Published simple sequence repeat data were re-analyzed to study population structure and the results were compared with the phylogenetic trees constructed using sequence data and coalescence simulations. (3) To distinguish between hybridization and incomplete lineage sorting, we developed and utilized a coalescence simulation approach. In other studies, species trees have been inferred despite the possibility of hybridization having occurred and used to generate distributions of the effect of lineage sorting alone (by coalescent simulation). Since this is problematic, we instead generate these distributions directly from observed gene trees. Of the six trees generated, we used the most resolved three to detect hybrids. We found that 11 of 33 samples appear to be affected by historical hybridization. Analysis of the remaining three genes supported the conclusions from the hybrid detection test.

Conclusions: We have identified or confirmed probable hybrid origins for several Citrus cultivars using three different approaches-gene phylogenies, population structure analysis and coalescence simulation. Hybridization and incomplete lineage sorting were identified primarily based on differences among gene phylogenies with reference to expectations via coalescence simulations. We conclude that identifying hybridization as a frequent cause of incongruence among gene trees is critical to correctly infer the phylogeny among species of Citrus.

Show MeSH
Null and observed genes tree-to-tree distance distributions.(A) Tree-to-tree distances between 20 trees drawn from the posterior distribution of each observed gene tree from one another (right hand side; 400 combinations per pair wise comparison) and the observed gene trees to 20 simulated gene trees that makes up the  distribution for each observed gene tree (left hand side). The position of the 80% critical value for each of the three  distributions is marked (blue: MDH, red: LGT and green: HYB asterisks; left hand side). The lower boundary of the 95% credibility interval of each observed pair of genes’ tree-to-tree distances are marked (purple: LGT-HYB, light blur: HYB-MDH and orange: HYB-LGT asterisks; right hand side). The test statistic, φ, is the distance between the closest left and right hand asterisks and does not overlap, thereby indicating a rejection of the  hypothesis of lineage sorting alone. (B) Tree-to-tree distances as in A, but after the removal of individuals with a putative hybrid origin. Asterisks also as in A. In this case, removal of individuals of putative hybrid origin results in a zero result for φ, thereby indicating that the  hypothesis of lineage sorting alone cannot be rejected. The interpretation is that those individuals that have been removed (compared to A) require an alternative explanation beyond lineage sorting in order to account for their incongruent placement among the three gene trees, whereas those that remain in B do not.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3713030&req=5

pone-0068410-g004: Null and observed genes tree-to-tree distance distributions.(A) Tree-to-tree distances between 20 trees drawn from the posterior distribution of each observed gene tree from one another (right hand side; 400 combinations per pair wise comparison) and the observed gene trees to 20 simulated gene trees that makes up the distribution for each observed gene tree (left hand side). The position of the 80% critical value for each of the three distributions is marked (blue: MDH, red: LGT and green: HYB asterisks; left hand side). The lower boundary of the 95% credibility interval of each observed pair of genes’ tree-to-tree distances are marked (purple: LGT-HYB, light blur: HYB-MDH and orange: HYB-LGT asterisks; right hand side). The test statistic, φ, is the distance between the closest left and right hand asterisks and does not overlap, thereby indicating a rejection of the hypothesis of lineage sorting alone. (B) Tree-to-tree distances as in A, but after the removal of individuals with a putative hybrid origin. Asterisks also as in A. In this case, removal of individuals of putative hybrid origin results in a zero result for φ, thereby indicating that the hypothesis of lineage sorting alone cannot be rejected. The interpretation is that those individuals that have been removed (compared to A) require an alternative explanation beyond lineage sorting in order to account for their incongruent placement among the three gene trees, whereas those that remain in B do not.

Mentions: New “gene” trees were simulated in Mesquite using 8,000 individuals (handled as haploids, thus individuals = gene copies). When distances among gene trees and their distributions were plotted, we found that φ >0 in each comparison, thereby rejecting the hypothesis of lineage sorting alone as the explanation of gene tree incongruence (Figure 4A).


A six nuclear gene phylogeny of Citrus (Rutaceae) taking into account hybridization and lineage sorting.

Ramadugu C, Pfeil BE, Keremane ML, Lee RF, Maureira-Butler IJ, Roose ML - PLoS ONE (2013)

Null and observed genes tree-to-tree distance distributions.(A) Tree-to-tree distances between 20 trees drawn from the posterior distribution of each observed gene tree from one another (right hand side; 400 combinations per pair wise comparison) and the observed gene trees to 20 simulated gene trees that makes up the  distribution for each observed gene tree (left hand side). The position of the 80% critical value for each of the three  distributions is marked (blue: MDH, red: LGT and green: HYB asterisks; left hand side). The lower boundary of the 95% credibility interval of each observed pair of genes’ tree-to-tree distances are marked (purple: LGT-HYB, light blur: HYB-MDH and orange: HYB-LGT asterisks; right hand side). The test statistic, φ, is the distance between the closest left and right hand asterisks and does not overlap, thereby indicating a rejection of the  hypothesis of lineage sorting alone. (B) Tree-to-tree distances as in A, but after the removal of individuals with a putative hybrid origin. Asterisks also as in A. In this case, removal of individuals of putative hybrid origin results in a zero result for φ, thereby indicating that the  hypothesis of lineage sorting alone cannot be rejected. The interpretation is that those individuals that have been removed (compared to A) require an alternative explanation beyond lineage sorting in order to account for their incongruent placement among the three gene trees, whereas those that remain in B do not.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3713030&req=5

pone-0068410-g004: Null and observed genes tree-to-tree distance distributions.(A) Tree-to-tree distances between 20 trees drawn from the posterior distribution of each observed gene tree from one another (right hand side; 400 combinations per pair wise comparison) and the observed gene trees to 20 simulated gene trees that makes up the distribution for each observed gene tree (left hand side). The position of the 80% critical value for each of the three distributions is marked (blue: MDH, red: LGT and green: HYB asterisks; left hand side). The lower boundary of the 95% credibility interval of each observed pair of genes’ tree-to-tree distances are marked (purple: LGT-HYB, light blur: HYB-MDH and orange: HYB-LGT asterisks; right hand side). The test statistic, φ, is the distance between the closest left and right hand asterisks and does not overlap, thereby indicating a rejection of the hypothesis of lineage sorting alone. (B) Tree-to-tree distances as in A, but after the removal of individuals with a putative hybrid origin. Asterisks also as in A. In this case, removal of individuals of putative hybrid origin results in a zero result for φ, thereby indicating that the hypothesis of lineage sorting alone cannot be rejected. The interpretation is that those individuals that have been removed (compared to A) require an alternative explanation beyond lineage sorting in order to account for their incongruent placement among the three gene trees, whereas those that remain in B do not.
Mentions: New “gene” trees were simulated in Mesquite using 8,000 individuals (handled as haploids, thus individuals = gene copies). When distances among gene trees and their distributions were plotted, we found that φ >0 in each comparison, thereby rejecting the hypothesis of lineage sorting alone as the explanation of gene tree incongruence (Figure 4A).

Bottom Line: We found that 11 of 33 samples appear to be affected by historical hybridization.Analysis of the remaining three genes supported the conclusions from the hybrid detection test.We conclude that identifying hybridization as a frequent cause of incongruence among gene trees is critical to correctly infer the phylogeny among species of Citrus.

View Article: PubMed Central - PubMed

Affiliation: Department of Botany and Plant Sciences, University of California Riverside, Riverside, California, United States of America.

ABSTRACT

Background: Genus Citrus (Rutaceae) comprises many important cultivated species that generally hybridize easily. Phylogenetic study of a group showing extensive hybridization is challenging. Since the genus Citrus has diverged recently (4-12 Ma), incomplete lineage sorting of ancestral polymorphisms is also likely to cause discrepancies among genes in phylogenetic inferences. Incongruence of gene trees is observed and it is essential to unravel the processes that cause inconsistencies in order to understand the phylogenetic relationships among the species.

Methodology and principal findings: (1) We generated phylogenetic trees using haplotype sequences of six low copy nuclear genes. (2) Published simple sequence repeat data were re-analyzed to study population structure and the results were compared with the phylogenetic trees constructed using sequence data and coalescence simulations. (3) To distinguish between hybridization and incomplete lineage sorting, we developed and utilized a coalescence simulation approach. In other studies, species trees have been inferred despite the possibility of hybridization having occurred and used to generate distributions of the effect of lineage sorting alone (by coalescent simulation). Since this is problematic, we instead generate these distributions directly from observed gene trees. Of the six trees generated, we used the most resolved three to detect hybrids. We found that 11 of 33 samples appear to be affected by historical hybridization. Analysis of the remaining three genes supported the conclusions from the hybrid detection test.

Conclusions: We have identified or confirmed probable hybrid origins for several Citrus cultivars using three different approaches-gene phylogenies, population structure analysis and coalescence simulation. Hybridization and incomplete lineage sorting were identified primarily based on differences among gene phylogenies with reference to expectations via coalescence simulations. We conclude that identifying hybridization as a frequent cause of incongruence among gene trees is critical to correctly infer the phylogeny among species of Citrus.

Show MeSH