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Species-Level Para-and Polyphyly in DNA Barcode Gene Trees: Strong Operational Bias in European Lepidoptera

The proliferation of DNA data is revolutionizing all fields of systematic research. DNA barcode sequences, now available for millions of specimens and several hundred thousand species, are increasingly used in algorithmic species delimitations. This is complicated by occasional incongruences between... Full description

Journal Title: Systematic biology 2016-11-01, Vol.65 (6), p.1024-1040
Main Author: Mutanen, M
Other Authors: Kivelä, S.M , Vos, Rutger , Doorenweerd, C , Ratnasingham, S , Hausmann, A , Huemer, P , Dinca, V , Nieukerken, Erik , Lopez-Vaamonde, C , Vila, R , Aarvik, L , Decaëns, T , Efetov, K.A , Hebert, P.D.N , Johnsen, A , Karsholt, O , Pentinsaari, M , Rougerie, R , Segerer, A , Tarmann, G , Zahiri, R , Godfray, H.C.J
Format: Electronic Article Electronic Article
Language: English
Subjects:
DNA
Quelle: Alma/SFX Local Collection
Publisher: England: Oxford University Press
ID: ISSN: 1063-5157
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recordid: cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5066064
title: Species-Level Para-and Polyphyly in DNA Barcode Gene Trees: Strong Operational Bias in European Lepidoptera
format: Article
creator:
  • Mutanen, M
  • Kivelä, S.M
  • Vos, Rutger
  • Doorenweerd, C
  • Ratnasingham, S
  • Hausmann, A
  • Huemer, P
  • Dinca, V
  • Nieukerken, Erik
  • Lopez-Vaamonde, C
  • Vila, R
  • Aarvik, L
  • Decaëns, T
  • Efetov, K.A
  • Hebert, P.D.N
  • Johnsen, A
  • Karsholt, O
  • Pentinsaari, M
  • Rougerie, R
  • Segerer, A
  • Tarmann, G
  • Zahiri, R
  • Godfray, H.C.J
subjects:
  • Allopatric species
  • Animals
  • arbre phylogénétique
  • atira
  • Bar codes
  • Bias
  • Biological taxonomies
  • Butterflies & moths
  • Classification - methods
  • code barre adn
  • Datasets
  • Deoxyribonucleic acid
  • DNA
  • DNA barcoding
  • DNA Barcoding, Taxonomic
  • DNA, Mitochondrial
  • Gene tree
  • Genes
  • Genes, Mitochondrial
  • Genetic variation
  • génome mitochondrial
  • identification des espèces
  • insecta
  • Journal Article
  • Lepidoptera
  • Lepidoptera - classification
  • Lepidoptera - genetics
  • Life Sciences
  • Mitochondrial COI
  • Mitochondrial cox1
  • mitochondrial DNA
  • molecular taxonomy
  • monophylie
  • Monophyly
  • paraphylie
  • Paraphyly
  • Phylogenetics
  • Phylogeny
  • polyphylie
  • Polyphyly
  • pubmedpublicationtype
  • pure
  • Regular
  • Regular Articles
  • researchoutput
  • Sampling
  • Species delimitation
  • species identification
  • Species monophyly
  • Specimens
  • Sympatric species
  • taxonomie moléculaire
ispartof: Systematic biology, 2016-11-01, Vol.65 (6), p.1024-1040
description: The proliferation of DNA data is revolutionizing all fields of systematic research. DNA barcode sequences, now available for millions of specimens and several hundred thousand species, are increasingly used in algorithmic species delimitations. This is complicated by occasional incongruences between species and gene genealogies, as indicated by situations where conspecific individuals do not form a monophyletic cluster in a gene tree. In two previous reviews, nonmonophyly has been reported as being common in mitochondrial DNA gene trees. We developed a novel web service "Monophylizer" to detect non-monophyly in phylogenetic trees and used it to ascertain the incidence of species nonmonophyly in COI (a.k.a. coxl) barcode sequence data from 4977 species and 41,583 specimens of European Lepidoptera, the largest data set of DNA barcodes analyzed from this regard. Particular attention was paid to accurate species identification to ensure data integrity. We investigated the effects of tree-building method, sampling effort, and other methodological issues, all of which can influence estimates of non-monophyly. We found a 12% incidence of non-monophyly, a value significantly lower than that observed in previous studies. Neighbor joining (NJ) and maximum likelihood (ML) methods yielded almost equal numbers of non-monophyletic species, but 24.1% of these cases of non-monophyly were only found by one of these methods. Non-monophyletic species tend to show either low genetic distances to their nearest neighbors or exceptionally high levels of intraspecific variability. Cases of polyphyly in COI trees arising as a result of deep intraspecific divergence are negligible, as the detected cases reflected misidentifications or methodological errors. Taking into consideration variation in sampling effort, we estimate that the true incidence of non-monophyly is ~23%, but with operational factors still being included. Within the operational factors, we separately assessed the frequency of taxonomic limitations (presence of overlooked cryptic and oversplit species) and identification uncertainties. We observed that operational factors are potentially present in more than half (58.6%) of the detected cases of non-monophyly. Furthermore, we observed that in about 20% of non-monophyletic species and entangled species, the lineages involved are either allopatric or parapatric—conditions where species delimitation is inherently subjective and particularly dependent on the species co
language: eng
source: Alma/SFX Local Collection
identifier: ISSN: 1063-5157
fulltext: fulltext
issn:
  • 1063-5157
  • 1076-836X
url: Link


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titleSpecies-Level Para-and Polyphyly in DNA Barcode Gene Trees: Strong Operational Bias in European Lepidoptera
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creatorMutanen, M ; Kivelä, S.M ; Vos, Rutger ; Doorenweerd, C ; Ratnasingham, S ; Hausmann, A ; Huemer, P ; Dinca, V ; Nieukerken, Erik ; Lopez-Vaamonde, C ; Vila, R ; Aarvik, L ; Decaëns, T ; Efetov, K.A ; Hebert, P.D.N ; Johnsen, A ; Karsholt, O ; Pentinsaari, M ; Rougerie, R ; Segerer, A ; Tarmann, G ; Zahiri, R ; Godfray, H.C.J
creatorcontribMutanen, M ; Kivelä, S.M ; Vos, Rutger ; Doorenweerd, C ; Ratnasingham, S ; Hausmann, A ; Huemer, P ; Dinca, V ; Nieukerken, Erik ; Lopez-Vaamonde, C ; Vila, R ; Aarvik, L ; Decaëns, T ; Efetov, K.A ; Hebert, P.D.N ; Johnsen, A ; Karsholt, O ; Pentinsaari, M ; Rougerie, R ; Segerer, A ; Tarmann, G ; Zahiri, R ; Godfray, H.C.J
descriptionThe proliferation of DNA data is revolutionizing all fields of systematic research. DNA barcode sequences, now available for millions of specimens and several hundred thousand species, are increasingly used in algorithmic species delimitations. This is complicated by occasional incongruences between species and gene genealogies, as indicated by situations where conspecific individuals do not form a monophyletic cluster in a gene tree. In two previous reviews, nonmonophyly has been reported as being common in mitochondrial DNA gene trees. We developed a novel web service "Monophylizer" to detect non-monophyly in phylogenetic trees and used it to ascertain the incidence of species nonmonophyly in COI (a.k.a. coxl) barcode sequence data from 4977 species and 41,583 specimens of European Lepidoptera, the largest data set of DNA barcodes analyzed from this regard. Particular attention was paid to accurate species identification to ensure data integrity. We investigated the effects of tree-building method, sampling effort, and other methodological issues, all of which can influence estimates of non-monophyly. We found a 12% incidence of non-monophyly, a value significantly lower than that observed in previous studies. Neighbor joining (NJ) and maximum likelihood (ML) methods yielded almost equal numbers of non-monophyletic species, but 24.1% of these cases of non-monophyly were only found by one of these methods. Non-monophyletic species tend to show either low genetic distances to their nearest neighbors or exceptionally high levels of intraspecific variability. Cases of polyphyly in COI trees arising as a result of deep intraspecific divergence are negligible, as the detected cases reflected misidentifications or methodological errors. Taking into consideration variation in sampling effort, we estimate that the true incidence of non-monophyly is ~23%, but with operational factors still being included. Within the operational factors, we separately assessed the frequency of taxonomic limitations (presence of overlooked cryptic and oversplit species) and identification uncertainties. We observed that operational factors are potentially present in more than half (58.6%) of the detected cases of non-monophyly. Furthermore, we observed that in about 20% of non-monophyletic species and entangled species, the lineages involved are either allopatric or parapatric—conditions where species delimitation is inherently subjective and particularly dependent on the species concept that has been adopted. These observations suggest that species-level non-monophyly in COI gene trees is less common than previously supposed, with many cases reflecting misidentifications, the subjectivity of species delimitation or other operational factors.
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languageeng
publisherEngland: Oxford University Press
subjectAllopatric species ; Animals ; arbre phylogénétique ; atira ; Bar codes ; Bias ; Biological taxonomies ; Butterflies & moths ; Classification - methods ; code barre adn ; Datasets ; Deoxyribonucleic acid ; DNA ; DNA barcoding ; DNA Barcoding, Taxonomic ; DNA, Mitochondrial ; Gene tree ; Genes ; Genes, Mitochondrial ; Genetic variation ; génome mitochondrial ; identification des espèces ; insecta ; Journal Article ; Lepidoptera ; Lepidoptera - classification ; Lepidoptera - genetics ; Life Sciences ; Mitochondrial COI ; Mitochondrial cox1 ; mitochondrial DNA ; molecular taxonomy ; monophylie ; Monophyly ; paraphylie ; Paraphyly ; Phylogenetics ; Phylogeny ; polyphylie ; Polyphyly ; pubmedpublicationtype ; pure ; Regular ; Regular Articles ; researchoutput ; Sampling ; Species delimitation ; species identification ; Species monophyly ; Specimens ; Sympatric species ; taxonomie moléculaire
ispartofSystematic biology, 2016-11-01, Vol.65 (6), p.1024-1040
rights
0Copyright © 2016 Society of Systematic Biologists
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3The Author(s) 2016. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. 2016
4The Author(s) 2016. Published by Oxford University Press, on behalf of the Society of Systematic Biologists.
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1Kivelä, S.M
2Vos, Rutger
3Doorenweerd, C
4Ratnasingham, S
5Hausmann, A
6Huemer, P
7Dinca, V
8Nieukerken, Erik
9Lopez-Vaamonde, C
10Vila, R
11Aarvik, L
12Decaëns, T
13Efetov, K.A
14Hebert, P.D.N
15Johnsen, A
16Karsholt, O
17Pentinsaari, M
18Rougerie, R
19Segerer, A
20Tarmann, G
21Zahiri, R
22Godfray, H.C.J
title
0Species-Level Para-and Polyphyly in DNA Barcode Gene Trees: Strong Operational Bias in European Lepidoptera
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descriptionThe proliferation of DNA data is revolutionizing all fields of systematic research. DNA barcode sequences, now available for millions of specimens and several hundred thousand species, are increasingly used in algorithmic species delimitations. This is complicated by occasional incongruences between species and gene genealogies, as indicated by situations where conspecific individuals do not form a monophyletic cluster in a gene tree. In two previous reviews, nonmonophyly has been reported as being common in mitochondrial DNA gene trees. We developed a novel web service "Monophylizer" to detect non-monophyly in phylogenetic trees and used it to ascertain the incidence of species nonmonophyly in COI (a.k.a. coxl) barcode sequence data from 4977 species and 41,583 specimens of European Lepidoptera, the largest data set of DNA barcodes analyzed from this regard. Particular attention was paid to accurate species identification to ensure data integrity. We investigated the effects of tree-building method, sampling effort, and other methodological issues, all of which can influence estimates of non-monophyly. We found a 12% incidence of non-monophyly, a value significantly lower than that observed in previous studies. Neighbor joining (NJ) and maximum likelihood (ML) methods yielded almost equal numbers of non-monophyletic species, but 24.1% of these cases of non-monophyly were only found by one of these methods. Non-monophyletic species tend to show either low genetic distances to their nearest neighbors or exceptionally high levels of intraspecific variability. Cases of polyphyly in COI trees arising as a result of deep intraspecific divergence are negligible, as the detected cases reflected misidentifications or methodological errors. Taking into consideration variation in sampling effort, we estimate that the true incidence of non-monophyly is ~23%, but with operational factors still being included. Within the operational factors, we separately assessed the frequency of taxonomic limitations (presence of overlooked cryptic and oversplit species) and identification uncertainties. We observed that operational factors are potentially present in more than half (58.6%) of the detected cases of non-monophyly. Furthermore, we observed that in about 20% of non-monophyletic species and entangled species, the lineages involved are either allopatric or parapatric—conditions where species delimitation is inherently subjective and particularly dependent on the species concept that has been adopted. These observations suggest that species-level non-monophyly in COI gene trees is less common than previously supposed, with many cases reflecting misidentifications, the subjectivity of species delimitation or other operational factors.
subject
0Allopatric species
1Animals
2arbre phylogénétique
3atira
4Bar codes
5Bias
6Biological taxonomies
7Butterflies & moths
8Classification - methods
9code barre adn
10Datasets
11Deoxyribonucleic acid
12DNA
13DNA barcoding
14DNA Barcoding, Taxonomic
15DNA, Mitochondrial
16Gene tree
17Genes
18Genes, Mitochondrial
19Genetic variation
20génome mitochondrial
21identification des espèces
22insecta
23Journal Article
24Lepidoptera
25Lepidoptera - classification
26Lepidoptera - genetics
27Life Sciences
28Mitochondrial COI
29Mitochondrial cox1
30mitochondrial DNA
31molecular taxonomy
32monophylie
33Monophyly
34paraphylie
35Paraphyly
36Phylogenetics
37Phylogeny
38polyphylie
39Polyphyly
40pubmedpublicationtype
41pure
42Regular
43Regular Articles
44researchoutput
45Sampling
46Species delimitation
47species identification
48Species monophyly
49Specimens
50Sympatric species
51taxonomie moléculaire
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8Nieukerken, Erik
9Lopez-Vaamonde, C
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titleSpecies-Level Para-and Polyphyly in DNA Barcode Gene Trees: Strong Operational Bias in European Lepidoptera
authorMutanen, M ; Kivelä, S.M ; Vos, Rutger ; Doorenweerd, C ; Ratnasingham, S ; Hausmann, A ; Huemer, P ; Dinca, V ; Nieukerken, Erik ; Lopez-Vaamonde, C ; Vila, R ; Aarvik, L ; Decaëns, T ; Efetov, K.A ; Hebert, P.D.N ; Johnsen, A ; Karsholt, O ; Pentinsaari, M ; Rougerie, R ; Segerer, A ; Tarmann, G ; Zahiri, R ; Godfray, H.C.J
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7Butterflies & moths
8Classification - methods
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36Phylogenetics
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42Regular
43Regular Articles
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45Sampling
46Species delimitation
47species identification
48Species monophyly
49Specimens
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51taxonomie moléculaire
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issn1063-5157
eissn1076-836X
abstractThe proliferation of DNA data is revolutionizing all fields of systematic research. DNA barcode sequences, now available for millions of specimens and several hundred thousand species, are increasingly used in algorithmic species delimitations. This is complicated by occasional incongruences between species and gene genealogies, as indicated by situations where conspecific individuals do not form a monophyletic cluster in a gene tree. In two previous reviews, nonmonophyly has been reported as being common in mitochondrial DNA gene trees. We developed a novel web service "Monophylizer" to detect non-monophyly in phylogenetic trees and used it to ascertain the incidence of species nonmonophyly in COI (a.k.a. coxl) barcode sequence data from 4977 species and 41,583 specimens of European Lepidoptera, the largest data set of DNA barcodes analyzed from this regard. Particular attention was paid to accurate species identification to ensure data integrity. We investigated the effects of tree-building method, sampling effort, and other methodological issues, all of which can influence estimates of non-monophyly. We found a 12% incidence of non-monophyly, a value significantly lower than that observed in previous studies. Neighbor joining (NJ) and maximum likelihood (ML) methods yielded almost equal numbers of non-monophyletic species, but 24.1% of these cases of non-monophyly were only found by one of these methods. Non-monophyletic species tend to show either low genetic distances to their nearest neighbors or exceptionally high levels of intraspecific variability. Cases of polyphyly in COI trees arising as a result of deep intraspecific divergence are negligible, as the detected cases reflected misidentifications or methodological errors. Taking into consideration variation in sampling effort, we estimate that the true incidence of non-monophyly is ~23%, but with operational factors still being included. Within the operational factors, we separately assessed the frequency of taxonomic limitations (presence of overlooked cryptic and oversplit species) and identification uncertainties. We observed that operational factors are potentially present in more than half (58.6%) of the detected cases of non-monophyly. Furthermore, we observed that in about 20% of non-monophyletic species and entangled species, the lineages involved are either allopatric or parapatric—conditions where species delimitation is inherently subjective and particularly dependent on the species concept that has been adopted. These observations suggest that species-level non-monophyly in COI gene trees is less common than previously supposed, with many cases reflecting misidentifications, the subjectivity of species delimitation or other operational factors.
copEngland
pubOxford University Press
pmid27288478
doi10.1093/sysbio/syw044
orcidid
0https://orcid.org/0000-0003-2278-2368
1https://orcid.org/0000-0002-0418-4439
2https://orcid.org/0000-0002-2447-4388
3https://orcid.org/0000-0003-0915-3882
4https://orcid.org/0000-0003-0937-2815
oafree_for_read