Geographic patterns of mtDNA and Z-linked sequence variation in the Common Chiffchaff and the ‘chiffchaff complex’

Marko Raković (Corresponding Author), Júlio M. Neto, Ricardo J. Lopes, Evgeniy A. Koblik, Igor V. Fadeev, Yuriy V. Lohman, Sargis A. Aghayan, Giovanni Boano, Marco Pavia, Yoav Perlman, Yosef Kiat, Amir Ben Dov, J. Martin Collinson, Gary Voelker, Sergei V. Drovetski

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Abstract

The Common Chiffchaff Phylloscopus collybita is an abundant, polytypic Palearctic bird. Validity of some of its subspecies is controversial and birds from some parts of the species range remain unclassified taxonomically. The relationships among populations from different geographic areas have not been sufficiently explored with molecular data. In this study we analyzed the relationships among the four species in the ‘chiffchaff complex’ (Common Chiffchaff, Iberian Chiffchaff P. ibericus, Canary Islands Chiffchaff P. canariensis and Mountain Chiffchaff P. sindianus), and the patterns of intraspecific geographic variation in the mtDNA ND2 gene and intron 9 of the Z-linked aconitase gene (ACO1I9) across the Common Chiffchaff range, including a recently discovered population breeding on Mt. Hermon (Anti-Lebanon mountains). Our data supported the monophyly of the chiffchaff complex and its current systematics at the species level. Within the Common Chiffchaff, the Siberian race P. c. tristis was the most differentiated subspecies and may represent a separate or incipient species. Other Common Chiffchaff subspecies also were differentiated in their mtDNA, however, lineages of neighboring subspecies formed wide zones of introgression. The Mt. Hermon population was of mixed genetic origin but contained some birds with novel unique lineage that could not be assigned to known subspecies. All Common Chiffchaff lineages diverged at the end of the Ionian stage of Pleistocene. Lineage sorting of ACO1I9 alleles was not as complete as that of mtDNA. Chiffchaff species were mostly distinct at ACO1I9, except the Common and Canary Islands Chiffchaffs that shared multiple alleles. An AMOVA identified geographic structure in Common Chiffchaff ACO1I9 variation that was broadly consistent with that of mtDNA ND2 gene. The genetic and other data suggest the chiffchaff complex to be a group of evolutionarily young taxa that represent a paradigm of ‘species evolution in action’ from intergrading subspecies through to apparently complete biological speciation.
Original languageEnglish
Article numbere0210268
Number of pages20
JournalPloS ONE
Volume14
Issue number1
DOIs
Publication statusPublished - 4 Jan 2019

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Mitochondrial DNA
Birds
mitochondrial DNA
Genes
Canary Islands
Spain
birds
Alleles
mountains
Aconitate Hydratase
Population
aconitate hydratase
Lebanon
alleles
biological speciation
genes
geographical variation
Sorting
monophyly
sorting

Keywords

  • STATISTICAL-METHOD
  • POPULATION
  • SPECIATION
  • PHYLOGENY
  • DIFFERENTIATION
  • HYPOTHESIS
  • TIMESCALE
  • BIRDS

Cite this

Raković, M., Neto, J. M., Lopes, R. J., Koblik, E. A., Fadeev, I. V., Lohman, Y. V., ... Drovetski, S. V. (2019). Geographic patterns of mtDNA and Z-linked sequence variation in the Common Chiffchaff and the ‘chiffchaff complex’. PloS ONE, 14(1), [e0210268]. https://doi.org/10.1371/journal.pone.0210268

Geographic patterns of mtDNA and Z-linked sequence variation in the Common Chiffchaff and the ‘chiffchaff complex’. / Raković, Marko (Corresponding Author); Neto, Júlio M.; Lopes, Ricardo J.; Koblik, Evgeniy A.; Fadeev, Igor V.; Lohman, Yuriy V.; Aghayan, Sargis A.; Boano, Giovanni; Pavia, Marco; Perlman, Yoav; Kiat, Yosef; Dov, Amir Ben; Collinson, J. Martin; Voelker, Gary; Drovetski, Sergei V.

In: PloS ONE, Vol. 14, No. 1, e0210268, 04.01.2019.

Research output: Contribution to journalArticle

Raković, M, Neto, JM, Lopes, RJ, Koblik, EA, Fadeev, IV, Lohman, YV, Aghayan, SA, Boano, G, Pavia, M, Perlman, Y, Kiat, Y, Dov, AB, Collinson, JM, Voelker, G & Drovetski, SV 2019, 'Geographic patterns of mtDNA and Z-linked sequence variation in the Common Chiffchaff and the ‘chiffchaff complex’', PloS ONE, vol. 14, no. 1, e0210268. https://doi.org/10.1371/journal.pone.0210268
Raković, Marko ; Neto, Júlio M. ; Lopes, Ricardo J. ; Koblik, Evgeniy A. ; Fadeev, Igor V. ; Lohman, Yuriy V. ; Aghayan, Sargis A. ; Boano, Giovanni ; Pavia, Marco ; Perlman, Yoav ; Kiat, Yosef ; Dov, Amir Ben ; Collinson, J. Martin ; Voelker, Gary ; Drovetski, Sergei V. / Geographic patterns of mtDNA and Z-linked sequence variation in the Common Chiffchaff and the ‘chiffchaff complex’. In: PloS ONE. 2019 ; Vol. 14, No. 1.
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abstract = "The Common Chiffchaff Phylloscopus collybita is an abundant, polytypic Palearctic bird. Validity of some of its subspecies is controversial and birds from some parts of the species range remain unclassified taxonomically. The relationships among populations from different geographic areas have not been sufficiently explored with molecular data. In this study we analyzed the relationships among the four species in the ‘chiffchaff complex’ (Common Chiffchaff, Iberian Chiffchaff P. ibericus, Canary Islands Chiffchaff P. canariensis and Mountain Chiffchaff P. sindianus), and the patterns of intraspecific geographic variation in the mtDNA ND2 gene and intron 9 of the Z-linked aconitase gene (ACO1I9) across the Common Chiffchaff range, including a recently discovered population breeding on Mt. Hermon (Anti-Lebanon mountains). Our data supported the monophyly of the chiffchaff complex and its current systematics at the species level. Within the Common Chiffchaff, the Siberian race P. c. tristis was the most differentiated subspecies and may represent a separate or incipient species. Other Common Chiffchaff subspecies also were differentiated in their mtDNA, however, lineages of neighboring subspecies formed wide zones of introgression. The Mt. Hermon population was of mixed genetic origin but contained some birds with novel unique lineage that could not be assigned to known subspecies. All Common Chiffchaff lineages diverged at the end of the Ionian stage of Pleistocene. Lineage sorting of ACO1I9 alleles was not as complete as that of mtDNA. Chiffchaff species were mostly distinct at ACO1I9, except the Common and Canary Islands Chiffchaffs that shared multiple alleles. An AMOVA identified geographic structure in Common Chiffchaff ACO1I9 variation that was broadly consistent with that of mtDNA ND2 gene. The genetic and other data suggest the chiffchaff complex to be a group of evolutionarily young taxa that represent a paradigm of ‘species evolution in action’ from intergrading subspecies through to apparently complete biological speciation.",
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note = "We are grateful to the University of Washington Burke Museum (UWBM), US National Museum of Natural History (USNM), National History Museum Belgrade (NHMBEO), State Darwin Museum (SDM), Zoological Museum of Moscow State University (MSUZM), Yale Peabody Museum (YPM), University of Minnesota Bell Museum (MMNH), Texas A&M University Biodiversity Research and Teaching Collections (TCWC), Staffan Bensch, Stephen Menzie and Nigel Odin for sample loans. This is publication number 1585 of the Biodiversity Research and Teaching Collections at Texas A&M University. Funding: This work was supported by FEDER funds through the COMPETE programme, POPH/QREN/FSE funds to S.V.D. and NORTE2020/PORTUGAL funds (NORTE-01-0145-FEDER-AGRIGEN) to R.J.L., by the Funda{\cc}{\~a}o para a Ci{\^e}ncia e a Tecnologia/MEC to S.V.D. (FCOMP-01-0124-FEDER-008941; PTDC/BIA- BEC/103435/2008) and R.J.L (SFRH/BPD/84141/2012), by the National Geographic Society to S.V.D, by Torino University Grant ex 60{\%} 2017 and 2018 to M. P. and by Ministarstvo Kulture I Informisanja Republike Srbije (Project: Ptice zapadnog palearktika) to M.R. The Russian Science Foundation grant No. 14-50-00029 'Scientific basis of the national biobank – depository of living systems' (to E.A.K). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The Russian Science Foundation grant No. 14-50-00029 'Scientific basis of the national biobank – depository of living systems' (to E.A.K).",
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T1 - Geographic patterns of mtDNA and Z-linked sequence variation in the Common Chiffchaff and the ‘chiffchaff complex’

AU - Raković, Marko

AU - Neto, Júlio M.

AU - Lopes, Ricardo J.

AU - Koblik, Evgeniy A.

AU - Fadeev, Igor V.

AU - Lohman, Yuriy V.

AU - Aghayan, Sargis A.

AU - Boano, Giovanni

AU - Pavia, Marco

AU - Perlman, Yoav

AU - Kiat, Yosef

AU - Dov, Amir Ben

AU - Collinson, J. Martin

AU - Voelker, Gary

AU - Drovetski, Sergei V.

N1 - We are grateful to the University of Washington Burke Museum (UWBM), US National Museum of Natural History (USNM), National History Museum Belgrade (NHMBEO), State Darwin Museum (SDM), Zoological Museum of Moscow State University (MSUZM), Yale Peabody Museum (YPM), University of Minnesota Bell Museum (MMNH), Texas A&M University Biodiversity Research and Teaching Collections (TCWC), Staffan Bensch, Stephen Menzie and Nigel Odin for sample loans. This is publication number 1585 of the Biodiversity Research and Teaching Collections at Texas A&M University. Funding: This work was supported by FEDER funds through the COMPETE programme, POPH/QREN/FSE funds to S.V.D. and NORTE2020/PORTUGAL funds (NORTE-01-0145-FEDER-AGRIGEN) to R.J.L., by the Fundação para a Ciência e a Tecnologia/MEC to S.V.D. (FCOMP-01-0124-FEDER-008941; PTDC/BIA- BEC/103435/2008) and R.J.L (SFRH/BPD/84141/2012), by the National Geographic Society to S.V.D, by Torino University Grant ex 60% 2017 and 2018 to M. P. and by Ministarstvo Kulture I Informisanja Republike Srbije (Project: Ptice zapadnog palearktika) to M.R. The Russian Science Foundation grant No. 14-50-00029 'Scientific basis of the national biobank – depository of living systems' (to E.A.K). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The Russian Science Foundation grant No. 14-50-00029 'Scientific basis of the national biobank – depository of living systems' (to E.A.K).

PY - 2019/1/4

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N2 - The Common Chiffchaff Phylloscopus collybita is an abundant, polytypic Palearctic bird. Validity of some of its subspecies is controversial and birds from some parts of the species range remain unclassified taxonomically. The relationships among populations from different geographic areas have not been sufficiently explored with molecular data. In this study we analyzed the relationships among the four species in the ‘chiffchaff complex’ (Common Chiffchaff, Iberian Chiffchaff P. ibericus, Canary Islands Chiffchaff P. canariensis and Mountain Chiffchaff P. sindianus), and the patterns of intraspecific geographic variation in the mtDNA ND2 gene and intron 9 of the Z-linked aconitase gene (ACO1I9) across the Common Chiffchaff range, including a recently discovered population breeding on Mt. Hermon (Anti-Lebanon mountains). Our data supported the monophyly of the chiffchaff complex and its current systematics at the species level. Within the Common Chiffchaff, the Siberian race P. c. tristis was the most differentiated subspecies and may represent a separate or incipient species. Other Common Chiffchaff subspecies also were differentiated in their mtDNA, however, lineages of neighboring subspecies formed wide zones of introgression. The Mt. Hermon population was of mixed genetic origin but contained some birds with novel unique lineage that could not be assigned to known subspecies. All Common Chiffchaff lineages diverged at the end of the Ionian stage of Pleistocene. Lineage sorting of ACO1I9 alleles was not as complete as that of mtDNA. Chiffchaff species were mostly distinct at ACO1I9, except the Common and Canary Islands Chiffchaffs that shared multiple alleles. An AMOVA identified geographic structure in Common Chiffchaff ACO1I9 variation that was broadly consistent with that of mtDNA ND2 gene. The genetic and other data suggest the chiffchaff complex to be a group of evolutionarily young taxa that represent a paradigm of ‘species evolution in action’ from intergrading subspecies through to apparently complete biological speciation.

AB - The Common Chiffchaff Phylloscopus collybita is an abundant, polytypic Palearctic bird. Validity of some of its subspecies is controversial and birds from some parts of the species range remain unclassified taxonomically. The relationships among populations from different geographic areas have not been sufficiently explored with molecular data. In this study we analyzed the relationships among the four species in the ‘chiffchaff complex’ (Common Chiffchaff, Iberian Chiffchaff P. ibericus, Canary Islands Chiffchaff P. canariensis and Mountain Chiffchaff P. sindianus), and the patterns of intraspecific geographic variation in the mtDNA ND2 gene and intron 9 of the Z-linked aconitase gene (ACO1I9) across the Common Chiffchaff range, including a recently discovered population breeding on Mt. Hermon (Anti-Lebanon mountains). Our data supported the monophyly of the chiffchaff complex and its current systematics at the species level. Within the Common Chiffchaff, the Siberian race P. c. tristis was the most differentiated subspecies and may represent a separate or incipient species. Other Common Chiffchaff subspecies also were differentiated in their mtDNA, however, lineages of neighboring subspecies formed wide zones of introgression. The Mt. Hermon population was of mixed genetic origin but contained some birds with novel unique lineage that could not be assigned to known subspecies. All Common Chiffchaff lineages diverged at the end of the Ionian stage of Pleistocene. Lineage sorting of ACO1I9 alleles was not as complete as that of mtDNA. Chiffchaff species were mostly distinct at ACO1I9, except the Common and Canary Islands Chiffchaffs that shared multiple alleles. An AMOVA identified geographic structure in Common Chiffchaff ACO1I9 variation that was broadly consistent with that of mtDNA ND2 gene. The genetic and other data suggest the chiffchaff complex to be a group of evolutionarily young taxa that represent a paradigm of ‘species evolution in action’ from intergrading subspecies through to apparently complete biological speciation.

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KW - POPULATION

KW - SPECIATION

KW - PHYLOGENY

KW - DIFFERENTIATION

KW - HYPOTHESIS

KW - TIMESCALE

KW - BIRDS

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