Collembola, the biological species concept and the underestimation of global species richness
Despite its ancient origin, global distribution and abundance in nearly all habitats, the class Collembola is comprised of only 8000 described species and is estimated to number no more than 50 000. Many morphologically defined species have broad geographical ranges that span continents, and recent...
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Published in | Molecular ecology Vol. 22; no. 21; pp. 5382 - 5396 |
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Main Authors | , , |
Format | Journal Article |
Language | English |
Published |
Oxford
Blackwell Publishing Ltd
01.11.2013
Blackwell |
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Abstract | Despite its ancient origin, global distribution and abundance in nearly all habitats, the class Collembola is comprised of only 8000 described species and is estimated to number no more than 50 000. Many morphologically defined species have broad geographical ranges that span continents, and recent molecular work has revealed high genetic diversity within species. However, the evolutionary significance of this genetic diversity is unknown. In this study, we sample five morphological species of the globally distributed genus Lepidocyrtus from 14 Panamanian sampling sites to characterize genetic diversity and test morphospecies against the biological species concept. Mitochondrial and nuclear DNA sequence data were analysed and a total of 58 molecular lineages revealed. Deep lineage diversification was recovered, with 30 molecular lineages estimated to have established more than 10 million years ago, and the origin almost all contemporary lineages preceding the onset of the Pleistocene (~2 Mya). Thirty‐four lineages were sampled in sympatry revealing unambiguous cosegregation of mitochondrial and nuclear DNA sequence variation, consistent with biological species. Species richness within the class Collembola and the geographical structure of this diversity are substantially misrepresented components of terrestrial animal biodiversity. We speculate that global species richness of Collembola could be at least an order of magnitude greater than a previous estimate of 50 000 species. |
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AbstractList | Abstract
Despite its ancient origin, global distribution and abundance in nearly all habitats, the class
C
ollembola is comprised of only 8000 described species and is estimated to number no more than 50 000. Many morphologically defined species have broad geographical ranges that span continents, and recent molecular work has revealed high genetic diversity within species. However, the evolutionary significance of this genetic diversity is unknown. In this study, we sample five morphological species of the globally distributed genus
L
epidocyrtus
from 14
P
anamanian sampling sites to characterize genetic diversity and test morphospecies against the biological species concept. Mitochondrial and nuclear
DNA
sequence data were analysed and a total of 58 molecular lineages revealed. Deep lineage diversification was recovered, with 30 molecular lineages estimated to have established more than 10 million years ago, and the origin almost all contemporary lineages preceding the onset of the Pleistocene (~2 Mya). Thirty‐four lineages were sampled in sympatry revealing unambiguous cosegregation of mitochondrial and nuclear
DNA
sequence variation, consistent with biological species. Species richness within the class
C
ollembola and the geographical structure of this diversity are substantially misrepresented components of terrestrial animal biodiversity. We speculate that global species richness of
C
ollembola could be at least an order of magnitude greater than a previous estimate of 50 000 species. Despite its ancient origin, global distribution and abundance in nearly all habitats, the class Collembola is comprised of only 8000 described species and is estimated to number no more than 50 000. Many morphologically defined species have broad geographical ranges that span continents, and recent molecular work has revealed high genetic diversity within species. However, the evolutionary significance of this genetic diversity is unknown. In this study, we sample five morphological species of the globally distributed genus Lepidocyrtus from 14 Panamanian sampling sites to characterize genetic diversity and test morphospecies against the biological species concept. Mitochondrial and nuclear DNA sequence data were analysed and a total of 58 molecular lineages revealed. Deep lineage diversification was recovered, with 30 molecular lineages estimated to have established more than 10 million years ago, and the origin almost all contemporary lineages preceding the onset of the Pleistocene (~2 Mya). Thirty‐four lineages were sampled in sympatry revealing unambiguous cosegregation of mitochondrial and nuclear DNA sequence variation, consistent with biological species. Species richness within the class Collembola and the geographical structure of this diversity are substantially misrepresented components of terrestrial animal biodiversity. We speculate that global species richness of Collembola could be at least an order of magnitude greater than a previous estimate of 50 000 species. Despite its ancient origin, global distribution and abundance in nearly all habitats, the class Collembola is comprised of only 8000 described species and is estimated to number no more than 50 000. Many morphologically defined species have broad geographical ranges that span continents, and recent molecular work has revealed high genetic diversity within species. However, the evolutionary significance of this genetic diversity is unknown. In this study, we sample five morphological species of the globally distributed genus Lepidocyrtus from 14 Panamanian sampling sites to characterize genetic diversity and test morphospecies against the biological species concept. Mitochondrial and nuclear DNA sequence data were analysed and a total of 58 molecular lineages revealed. Deep lineage diversification was recovered, with 30 molecular lineages estimated to have established more than 10 million years ago, and the origin almost all contemporary lineages preceding the onset of the Pleistocene (~2 Mya). Thirty-four lineages were sampled in sympatry revealing unambiguous cosegregation of mitochondrial and nuclear DNA sequence variation, consistent with biological species. Species richness within the class Collembola and the geographical structure of this diversity are substantially misrepresented components of terrestrial animal biodiversity. We speculate that global species richness of Collembola could be at least an order of magnitude greater than a previous estimate of 50 000 species. [PUBLICATION ABSTRACT] Despite its ancient origin, global distribution and abundance in nearly all habitats, the class Collembola is comprised of only 8000 described species and is estimated to number no more than 50,000. Many morphologically defined species have broad geographical ranges that span continents, and recent molecular work has revealed high genetic diversity within species. However, the evolutionary significance of this genetic diversity is unknown. In this study, we sample five morphological species of the globally distributed genus Lepidocyrtus from 14 Panamanian sampling sites to characterize genetic diversity and test morphospecies against the biological species concept. Mitochondrial and nuclear DNA sequence data were analysed and a total of 58 molecular lineages revealed. Deep lineage diversification was recovered, with 30 molecular lineages estimated to have established more than 10 million years ago, and the origin almost all contemporary lineages preceding the onset of the Pleistocene (~2 Mya). Thirty-four lineages were sampled in sympatry revealing unambiguous cosegregation of mitochondrial and nuclear DNA sequence variation, consistent with biological species. Species richness within the class Collembola and the geographical structure of this diversity are substantially misrepresented components of terrestrial animal biodiversity. We speculate that global species richness of Collembola could be at least an order of magnitude greater than a previous estimate of 50,000 species. |
Author | Cicconardi, Francesco Fanciulli, Pietro P. Emerson, Brent C. |
Author_xml | – sequence: 1 givenname: Francesco surname: Cicconardi fullname: Cicconardi, Francesco email: francicco@gmail.com organization: Department of Physics, University of Rome "La Sapienza", P.le A. Moro 5, 00185, Rome, Italy – sequence: 2 givenname: Pietro P. surname: Fanciulli fullname: Fanciulli, Pietro P. organization: Department of Life Sciences, University of Siena, Via Aldo Moro 2, 53100, Siena, Italy – sequence: 3 givenname: Brent C. surname: Emerson fullname: Emerson, Brent C. organization: Island Ecology and Evolution Research Group, IPNA-CSIC, 38206, La LagunaTenerife, Canary Islands, Spain |
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Copyright | 2013 John Wiley & Sons Ltd 2015 INIST-CNRS 2013 John Wiley & Sons Ltd. Copyright © 2013 John Wiley & Sons Ltd |
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Keywords | Concept Lepidocyrtus molecular lineage Arthropoda Insecta Tropical zone Panama Cryptic species Collembola Invertebrata Biodiversity Species richness biodiversity cryptic species |
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Notes | Leverhulme Trust ark:/67375/WNG-6CVHNL8F-J Italian Ministry of Education ArticleID:MEC12472 Fig. S1. Lepidocyrtus cf vexans. Fig. S2. Boxplots showing the distributions of pairwise p-distances (π) for mtDNA COII and nuclear EF1α sequence data from morphospecies within the genus Lepidocyrtus. Fig. S3. Stacked histograms summarising results of amova analyses of mtDNA COII and nuclear EF1α sequence data from morphospecies within the genus Lepidocyrtus. Fig. S4. Summary tree from Bayesian inference (BI) and maximum likelihood (ML) analyses of mtDNA COII sequence data from morphospecies within the genus Lepidocyrtus. Fig. S5. Summary tree from Bayesian inference (BI) and maximum likelihood (ML) analyses of nuclear EF1α sequence data from morphospecies within the genus Lepidocyrtus. Fig. S6. Boxplots showing the distributions of most recent common ancestor (MRCA) estimates for molecular lineages within morphospecies from the genus Lepidocyrtus sampled from three Panamanian geological subdivisions. Fig. S7. Boxplots showing the distributions of pairwise p-distances for mtDNA COII and nuclear EF1α sequences in sympatric and allopatric molecular lineages within morphospecies from the genus Lepidocyrtus.Data S1. COII dataset.Data S2. EF1α dataset.Data S3. Sample identification table. Smithsonian Institution Short-fellowship Program istex:862E568E6757FC8242ACD1235B9BF5F8D2F58369 ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
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Deharveng L (2004) Recent ad 2010; 10 2004; 20 2012; 124 2010; 19 2000; 130 2003; 115 2012; 3273 2013; 8 1996; 32 1979 1933; 27 1965; 2 2011; 366 2010; 27 2001; 294 2010; 26 2013; 16 1990 2006; 23 1967; 12 2000; 403 1987 2008; 25 1986 1942 1983a; 85 2008; 23 2007; 4 2012; 29 2012; 27 2010; 4 2008; 1769 1964; 71 2012a; 26 1971; 63 1989; 1 2000; 25 1997; 491 2010; 449 2006; 55 1995; 57 2004; 48 2010; 123 1971; 25 2009 2007 2000; 71 2006 2006; 4 2003 2010; 81 2012; 3570 1998; 21 2001; 68 2003; 135 2012; 109 2007; 16 1991; 5 1981; 291 2011; 108 2006; 42 2012; 3 2011; 3108 2004; 19 1986; 22 1983b; 19 1926; 63 1998; 7 2003; 301 1959; 10 2012b; 7 2005; 14 e_1_2_7_5_1 e_1_2_7_3_1 Detsis V (e_1_2_7_14_1) 2000; 130 e_1_2_7_9_1 Mateos E (e_1_2_7_39_1) 2012; 3273 e_1_2_7_19_1 e_1_2_7_60_1 e_1_2_7_17_1 e_1_2_7_62_1 Yoshii R (e_1_2_7_74_1) 1989; 1 e_1_2_7_15_1 e_1_2_7_41_1 e_1_2_7_43_1 e_1_2_7_11_1 e_1_2_7_45_1 e_1_2_7_68_1 e_1_2_7_47_1 e_1_2_7_26_1 Denis JR (e_1_2_7_13_1) 1933; 27 e_1_2_7_49_1 e_1_2_7_28_1 Oksanen J (e_1_2_7_46_1) 2007 Rapoport E (e_1_2_7_55_1) 1971; 25 Cutz‐Pool LQ (e_1_2_7_10_1) 2010; 81 e_1_2_7_73_1 Mari‐Mutt JA (e_1_2_7_32_1) 1983; 19 Christiansen K (e_1_2_7_7_1) 1971; 63 e_1_2_7_50_1 e_1_2_7_71_1 e_1_2_7_25_1 e_1_2_7_52_1 e_1_2_7_23_1 Mari‐Mutt JA (e_1_2_7_34_1) 1990 e_1_2_7_54_1 e_1_2_7_21_1 e_1_2_7_56_1 e_1_2_7_58_1 Hopkin SP (e_1_2_7_27_1) 1997; 491 e_1_2_7_4_1 Mateos E (e_1_2_7_37_1) 2011; 3108 e_1_2_7_8_1 Szeptycki A (e_1_2_7_66_1) 1979 e_1_2_7_18_1 e_1_2_7_16_1 e_1_2_7_61_1 e_1_2_7_2_1 e_1_2_7_42_1 e_1_2_7_63_1 e_1_2_7_12_1 e_1_2_7_44_1 Yosii R (e_1_2_7_75_1) 1959; 10 e_1_2_7_67_1 e_1_2_7_48_1 e_1_2_7_69_1 e_1_2_7_29_1 Rambaut A (e_1_2_7_53_1) 2007 Greenslade P (e_1_2_7_24_1) 1986 Mayr E (e_1_2_7_40_1) 1942 e_1_2_7_72_1 Mateos E (e_1_2_7_36_1) 2008; 1769 e_1_2_7_51_1 e_1_2_7_70_1 e_1_2_7_30_1 Mateos E (e_1_2_7_38_1) 2012; 3570 e_1_2_7_76_1 e_1_2_7_57_1 Chapman AD (e_1_2_7_6_1) 2009 Mari‐Mutt JA (e_1_2_7_31_1) 1983; 85 e_1_2_7_20_1 e_1_2_7_59_1 Szeptycki A (e_1_2_7_65_1) 1967; 12 Mari‐Mutt JA (e_1_2_7_35_1) 1996; 32 Swofford DL (e_1_2_7_64_1) 2003 Mari‐Mutt JA (e_1_2_7_33_1) 1986; 22 Gisin H (e_1_2_7_22_1) 1965; 2 |
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Snippet | Despite its ancient origin, global distribution and abundance in nearly all habitats, the class Collembola is comprised of only 8000 described species and is... Abstract Despite its ancient origin, global distribution and abundance in nearly all habitats, the class C ollembola is comprised of only 8000 described... |
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SubjectTerms | Animal and plant ecology Animal, plant and microbial ecology Animals Arthropods Arthropods - classification Arthropods - genetics Bayes Theorem Biodiversity Biological and medical sciences Biological evolution Cell Nucleus - genetics Collembola cryptic species DNA, Mitochondrial - genetics Evolutionary biology Fundamental and applied biological sciences. Psychology General aspects Genetic diversity Genetic Speciation Genetic Variation Genetics of eukaryotes. Biological and molecular evolution Insecta Invertebrates Lepidocyrtus Likelihood Functions Linkage Disequilibrium Mitochondrial DNA molecular lineage Molecular Sequence Data Panama Phylogeny Population genetics, reproduction patterns Sequence Analysis, DNA Sympatry Synecology |
Title | Collembola, the biological species concept and the underestimation of global species richness |
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