Demographic History of the Genus Pan Inferred from Whole Mitochondrial Genome Reconstructions

Irene Lobon; Serena Tucci; Marc de Manuel; Silvia Ghirotto; Andrea Benazzo; Javier Prado-Martinez; Belen Lorente-Galdos; Kiwoong Nam; Marc Dabad; Jessica Hernandez-Rodriguez; David Comas; Arcadi Navarro; Mikkel H. Schierup; Aida M Andrés; Guido Barbujani; Christina Hvilsom; Tomas Marques-Bonet

doi:10.1093/gbe/evw124

Demographic History of the Genus Pan Inferred from Whole Mitochondrial Genome Reconstructions

Irene Lobon, Serena Tucci, Marc de Manuel, Silvia Ghirotto, Andrea Benazzo, Javier Prado-Martinez, Belen Lorente-Galdos, Kiwoong Nam, Marc Dabad, Jessica Hernandez-Rodriguez, David Comas, Arcadi Navarro, Mikkel H. Schierup, Aida M Andrés, Guido Barbujani, Christina Hvilsom, Tomas Marques-Bonet^*

^*Corresponding author for this work

Department of Molecular Biology and Genetics - Bioinformatics Research Centre (BiRC)

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

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Abstract

The genus Pan is the closest genus to our own and it includes two species, Panpaniscus ( bonobos) and Pan troglodytes ( chimpanzees). The later is constituted by four subspecies, all highly endangered. The study of the Pan genera has been incessantly complicated by the intricate relationship among subspecies and the statistical limitations imposed by the reduced number of samples or genomic markers analyzed. Here, we present a new method to reconstruct complete mitochondrial genomes ( mitogenomes) from whole genome shotgun ( WGS) datasets, mtArchitect, showing that its reconstructions are highly accurate and consistent with long-range PCR mitogenomes. We used this approach to build the mitochondrial genomes of 20 newly sequenced samples which, together with available genomes, allowed us to analyze the hitherto most complete Pan mitochondrial genome dataset including 156 chimpanzee and 44 bonobo individuals, with a proportional contribution from all chimpanzee subspecies. We estimated the separation time between chimpanzees and bonobos around 1.15 million years ago ( Mya) [ 0.81-1.49]. Further, we found that under the most probable genealogical model the two clades of chimpanzees, Western + Nigeria-Cameroon and Central + Eastern, separated at 0.59 Mya [ 0.41-0.78] with further internal separations at 0.32 Mya [ 0.22-0.43] and 0.16 Mya [ 0.17-0.34], respectively. Finally, for a subset of our samples, we compared nuclear versus mitochondrial genomes and we found that chimpanzee subspecies have different patterns of nuclear and mitochondrial diversity, which could be a result of either processes affecting the mitochondrial genome, such as hitchhiking or background selection, or a result of population dynamics.

Original language	English
Journal	Genome Biology and Evolution
Volume	8
Issue	6
Pages (from-to)	2020-2030
Number of pages	11
ISSN	1759-6653
DOIs	https://doi.org/10.1093/gbe/evw124
Publication status	Published - Jun 2016

Keywords

genome diversity
chimpanzee
bonobo
bioinformatics
next-generation sequencing
mtArchitect
POPULATION-GENETICS
DNA POLYMORPHISM
DIVERGENCE TIMES
GREAT APE
CHIMPANZEE
DIVERSITY
EVOLUTION
ALIGNMENT
PANISCUS
ARCHITECTURE

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evw124Final published version, 962 KBLicence: CC BY-NC

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Lobon, I., Tucci, S., de Manuel, M., Ghirotto, S., Benazzo, A., Prado-Martinez, J., Lorente-Galdos, B., Nam, K., Dabad, M., Hernandez-Rodriguez, J., Comas, D., Navarro, A., Schierup, M. H., Andrés, A. M., Barbujani, G., Hvilsom, C., & Marques-Bonet, T. (2016). Demographic History of the Genus Pan Inferred from Whole Mitochondrial Genome Reconstructions. Genome Biology and Evolution, 8(6), 2020-2030. https://doi.org/10.1093/gbe/evw124

@article{b802eb140c6249d9993092f229ecf13d,

title = "Demographic History of the Genus Pan Inferred from Whole Mitochondrial Genome Reconstructions",

abstract = "The genus Pan is the closest genus to our own and it includes two species, Panpaniscus ( bonobos) and Pan troglodytes ( chimpanzees). The later is constituted by four subspecies, all highly endangered. The study of the Pan genera has been incessantly complicated by the intricate relationship among subspecies and the statistical limitations imposed by the reduced number of samples or genomic markers analyzed. Here, we present a new method to reconstruct complete mitochondrial genomes ( mitogenomes) from whole genome shotgun ( WGS) datasets, mtArchitect, showing that its reconstructions are highly accurate and consistent with long-range PCR mitogenomes. We used this approach to build the mitochondrial genomes of 20 newly sequenced samples which, together with available genomes, allowed us to analyze the hitherto most complete Pan mitochondrial genome dataset including 156 chimpanzee and 44 bonobo individuals, with a proportional contribution from all chimpanzee subspecies. We estimated the separation time between chimpanzees and bonobos around 1.15 million years ago ( Mya) [ 0.81-1.49]. Further, we found that under the most probable genealogical model the two clades of chimpanzees, Western + Nigeria-Cameroon and Central + Eastern, separated at 0.59 Mya [ 0.41-0.78] with further internal separations at 0.32 Mya [ 0.22-0.43] and 0.16 Mya [ 0.17-0.34], respectively. Finally, for a subset of our samples, we compared nuclear versus mitochondrial genomes and we found that chimpanzee subspecies have different patterns of nuclear and mitochondrial diversity, which could be a result of either processes affecting the mitochondrial genome, such as hitchhiking or background selection, or a result of population dynamics.",

keywords = "genome diversity, chimpanzee, bonobo, bioinformatics, next-generation sequencing, mtArchitect, POPULATION-GENETICS, DNA POLYMORPHISM, DIVERGENCE TIMES, GREAT APE, CHIMPANZEE, DIVERSITY, EVOLUTION, ALIGNMENT, PANISCUS, ARCHITECTURE",

author = "Irene Lobon and Serena Tucci and {de Manuel}, Marc and Silvia Ghirotto and Andrea Benazzo and Javier Prado-Martinez and Belen Lorente-Galdos and Kiwoong Nam and Marc Dabad and Jessica Hernandez-Rodriguez and David Comas and Arcadi Navarro and Schierup, {Mikkel H.} and Andr{\'e}s, {Aida M} and Guido Barbujani and Christina Hvilsom and Tomas Marques-Bonet",

year = "2016",

month = jun,

doi = "10.1093/gbe/evw124",

language = "English",

volume = "8",

pages = "2020--2030",

journal = "Genome Biology and Evolution",

issn = "1759-6653",

publisher = "Oxford University Press",

number = "6",

}

Lobon, I, Tucci, S, de Manuel, M, Ghirotto, S, Benazzo, A, Prado-Martinez, J, Lorente-Galdos, B, Nam, K, Dabad, M, Hernandez-Rodriguez, J, Comas, D, Navarro, A, Schierup, MH, Andrés, AM, Barbujani, G, Hvilsom, C & Marques-Bonet, T 2016, 'Demographic History of the Genus Pan Inferred from Whole Mitochondrial Genome Reconstructions', Genome Biology and Evolution, vol. 8, no. 6, pp. 2020-2030. https://doi.org/10.1093/gbe/evw124

Demographic History of the Genus Pan Inferred from Whole Mitochondrial Genome Reconstructions. / Lobon, Irene; Tucci, Serena; de Manuel, Marc et al.
In: Genome Biology and Evolution, Vol. 8, No. 6, 06.2016, p. 2020-2030.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - Demographic History of the Genus Pan Inferred from Whole Mitochondrial Genome Reconstructions

AU - Lobon, Irene

AU - Tucci, Serena

AU - de Manuel, Marc

AU - Ghirotto, Silvia

AU - Benazzo, Andrea

AU - Prado-Martinez, Javier

AU - Lorente-Galdos, Belen

AU - Nam, Kiwoong

AU - Dabad, Marc

AU - Hernandez-Rodriguez, Jessica

AU - Comas, David

AU - Navarro, Arcadi

AU - Schierup, Mikkel H.

AU - Andrés, Aida M

AU - Barbujani, Guido

AU - Hvilsom, Christina

AU - Marques-Bonet, Tomas

PY - 2016/6

Y1 - 2016/6

N2 - The genus Pan is the closest genus to our own and it includes two species, Panpaniscus ( bonobos) and Pan troglodytes ( chimpanzees). The later is constituted by four subspecies, all highly endangered. The study of the Pan genera has been incessantly complicated by the intricate relationship among subspecies and the statistical limitations imposed by the reduced number of samples or genomic markers analyzed. Here, we present a new method to reconstruct complete mitochondrial genomes ( mitogenomes) from whole genome shotgun ( WGS) datasets, mtArchitect, showing that its reconstructions are highly accurate and consistent with long-range PCR mitogenomes. We used this approach to build the mitochondrial genomes of 20 newly sequenced samples which, together with available genomes, allowed us to analyze the hitherto most complete Pan mitochondrial genome dataset including 156 chimpanzee and 44 bonobo individuals, with a proportional contribution from all chimpanzee subspecies. We estimated the separation time between chimpanzees and bonobos around 1.15 million years ago ( Mya) [ 0.81-1.49]. Further, we found that under the most probable genealogical model the two clades of chimpanzees, Western + Nigeria-Cameroon and Central + Eastern, separated at 0.59 Mya [ 0.41-0.78] with further internal separations at 0.32 Mya [ 0.22-0.43] and 0.16 Mya [ 0.17-0.34], respectively. Finally, for a subset of our samples, we compared nuclear versus mitochondrial genomes and we found that chimpanzee subspecies have different patterns of nuclear and mitochondrial diversity, which could be a result of either processes affecting the mitochondrial genome, such as hitchhiking or background selection, or a result of population dynamics.

AB - The genus Pan is the closest genus to our own and it includes two species, Panpaniscus ( bonobos) and Pan troglodytes ( chimpanzees). The later is constituted by four subspecies, all highly endangered. The study of the Pan genera has been incessantly complicated by the intricate relationship among subspecies and the statistical limitations imposed by the reduced number of samples or genomic markers analyzed. Here, we present a new method to reconstruct complete mitochondrial genomes ( mitogenomes) from whole genome shotgun ( WGS) datasets, mtArchitect, showing that its reconstructions are highly accurate and consistent with long-range PCR mitogenomes. We used this approach to build the mitochondrial genomes of 20 newly sequenced samples which, together with available genomes, allowed us to analyze the hitherto most complete Pan mitochondrial genome dataset including 156 chimpanzee and 44 bonobo individuals, with a proportional contribution from all chimpanzee subspecies. We estimated the separation time between chimpanzees and bonobos around 1.15 million years ago ( Mya) [ 0.81-1.49]. Further, we found that under the most probable genealogical model the two clades of chimpanzees, Western + Nigeria-Cameroon and Central + Eastern, separated at 0.59 Mya [ 0.41-0.78] with further internal separations at 0.32 Mya [ 0.22-0.43] and 0.16 Mya [ 0.17-0.34], respectively. Finally, for a subset of our samples, we compared nuclear versus mitochondrial genomes and we found that chimpanzee subspecies have different patterns of nuclear and mitochondrial diversity, which could be a result of either processes affecting the mitochondrial genome, such as hitchhiking or background selection, or a result of population dynamics.

KW - genome diversity

KW - chimpanzee

KW - bonobo

KW - bioinformatics

KW - next-generation sequencing

KW - mtArchitect

KW - POPULATION-GENETICS

KW - DNA POLYMORPHISM

KW - DIVERGENCE TIMES

KW - GREAT APE

KW - CHIMPANZEE

KW - DIVERSITY

KW - EVOLUTION

KW - ALIGNMENT

KW - PANISCUS

KW - ARCHITECTURE

U2 - 10.1093/gbe/evw124

DO - 10.1093/gbe/evw124

M3 - Journal article

C2 - 27345955

SN - 1759-6653

VL - 8

SP - 2020

EP - 2030

JO - Genome Biology and Evolution

JF - Genome Biology and Evolution

IS - 6

ER -

Demographic History of the Genus Pan Inferred from Whole Mitochondrial Genome Reconstructions

Abstract

Keywords

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