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Genetic Calibration of Species Diversity Among North Americats

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Genetic Calibration of Species Diversity Among North Americats Genetic calibration of species diversity among North America’s freshwater fishes Julien Aprila,1, Richard L. Maydenb, Robert H. Hannerc, and Louis Bernatcheza aInstitut de Biologie Intégrative et des Systèmes, Université Laval, Quebec, QC, Canada G1V 0A6; bDepartment of Biology, Saint Louis University, Saint Louis, MO 63103; and cBiodiversity Institute of Ontario, University of Guelph, Guelph, ON, Canada N1G 2W1 Edited by Hugh MacIsaac, University of Windsor, Windsor, ON, Canada, and accepted by the Editorial Board May 7, 2011 (received for review November 4, 2010) Freshwater ecosystems are being heavily exploited and degraded tochrome c oxidase subunit I (COI) sequences have revealed by human activities all over the world, including in North America, cryptic diversity across the animal kingdom. For instance, pre- where fishes and fisheries are strongly affected. Despite centuries vious DNA barcoding studies in other taxonomic groups have of taxonomic inquiry, problems inherent to species identification found as many as nine undescribed species embedded within continue to hamper the conservation of North American freshwa- a single known species of skipper butterfly (11). These numbers ter fishes. Indeed, nearly 10% of species diversity is thought to are even larger in less studied groups, such as parasitic hyme- remain undescribed. To provide an independent calibration of tax- nopterans (12). Whereas many species may need to be split into onomic uncertainty and to establish a more accessible molecular distinct evolutionary lineages, others may need to be combined, identification key for its application, we generated a standard given that not all morphological differences are the result of reference library of mtDNA sequences (DNA barcodes) derived cladogenesis. In an outstanding case documented in fishes, in- from expert-identified museum specimens for 752 North American dividuals that belonged to two different species were found to be freshwater fish species. This study demonstrates that 90% of the female and male of a single species (13). known species can be delineated using barcodes. Moreover, it In this study, we established a barcode reference library for reveals numerous genetic discontinuities indicative of indepen- more than 80% of the named freshwater fish species of North dently evolving lineages within described species, which points to America. We used this survey of standing genetic diversity as an the presence of morphologically cryptic diversity. From the 752 independent calibration of current taxonomic resolution within species analyzed, our survey flagged 138 named species that rep- the North American fish fauna to reveal key areas of uncertainty resent as many as 347 candidate species, which suggests a 28% where discrepancies between genetic data and morphologically increase in species diversity. In contrast, several species of parasitic based taxonomy arise. In contrast, where DNA sequences and and nonparasitic lampreys lack such discontinuity and may repre- traditional taxonomy exhibit congruence, our data serve as an sent alternative life history strategies within single species. accessible key for the molecular identification of North Ameri- Therefore, it appears that the current North American freshwater can freshwater fishes. fish taxonomy at the species level significantly conceals diversity in some groups, although artificially creating diversity in others. In Results addition to providing an easily accessible digital identification We obtained mitochondrial barcodes for 5,674 fish specimens system, this study identifies 151 fish species for which taxonomic belonging to 50 families, 178 genera, and 752 species (Table 1). revision is required. This coverage includes more than 80% of the 902 Canadian and American species listed by Nelson et al. (14). In accordance with DNA barcoding | cytochrome c oxidase I | biodiversity | evolutionarily the Fish Barcode of Life Campaign (15), we deposited all se- significant units | aquatic ecosystem quences and collateral specimen information within the Barcode of Life Data System (BOLD) (16), where this information can be queried by users, annotated, and curated in light of new in- ssessing the state of life in a world that faces a sixth mass formation. This list of 752 species also includes 22 exotic invasive extinction (1, 2) represents one of the largest challenges of A species (non-native species that adversely affect ecosystems), 4 modern science. This assessment is particularly needed for North species closely related to North American species, and 30 world- American freshwater fishes. Indeed, 40% of the fauna is in peril wide species of lampreys (17) because those species are notori- (3), and it continues to support a multibillion dollar commercial ously difficult to identify and can have important ecological and and recreational fishery (4). Despite more than 2 centuries of economic impacts. For most species, multiple specimens (mean = descriptive taxonomic inquiry, problems inherent to species iden- 7.5 specimens per species) from distant localities (mean = 3.2 tification have hampered the study, conservation, and manage- localities per species) were analyzed to document intraspecific ment of the richest diversity of temperate freshwater fish (5). variability. Only 62 species were represented by a single specimen, Indeed, the exact amount of diversity is still unknown, and it is and 1 species (Etheostoma radiosum) was represented by 108 thought that 10% of North American freshwater fish are still specimens. We observed a hierarchical increase in mean di- formally undescribed (6, 7). Part of this problem may stem from the fact that there is no universally accepted operational species concept (8, 9). Most biologists agree that species are inde- pendently evolving lineages of populations or metapopulations Author contributions: J.A., R.L.M., R.H.H., and L.B. designed research; J.A., R.L.M., R.H.H., and L.B. performed research; J.A. and R.L.M. analyzed data; and J.A. wrote the paper. (8, 9), but a debate surrounds the choice of an exact cutoff in the fl divergence continuum. Morphological differentiation has long The authors declare no con ict of interest. been the criterion of choice for taxonomists because of the rel- This article is a PNAS Direct Submission. H.M. is a guest editor invited by the Editorial Board. ative ease with which those characters are assessed. Unfortu- Data deposition: The sequences reported in this paper have been deposited in the Gen- nately, such differences are not always caused by independent Bank database (for accession nos. see SI Materials and Methods). They have also been evolutionary history, and reproductively isolated taxa can some- deposited in Barcode of Life Data System (http://www.boldsystems.org) (projects Fresh- times be morphologically indistinguishable. water fishes of North America and Barcoding of Canadian freshwater fishes). Generating rapid and accurate molecular identifications using 1To whom correspondence should be addressed. E-mail: [email protected]. standardized tools can help to resolve distorted views of bio- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. diversity. Indeed, DNA barcoding (10) surveys using partial cy- 1073/pnas.1016437108/-/DCSupplemental. 10602–10607 | PNAS | June 28, 2011 | vol. 108 | no. 26 www.pnas.org/cgi/doi/10.1073/pnas.1016437108 Downloaded by guest on September 29, 2021 Table 1. Summary of the fish taxa analyzed est neighbor was 7.82 times higher than the mean intraspe- fi Species ci c divergence. The resolution of named species using barcodes approached Indistinguishable 90% (676 of 752) (Table 1, Table S1,andSI Text). Those de- Family Barcoded using barcodes With UCS (no. of UCS) lineated species could be identified using a diagnostic nucleo- tide approach (18) and were represented by a unique haplotype, Cyprinidae 221 10 52 (121) a single tight cluster of haplotypes, or distinct clusters of hap- Percidae 197 18 45 (120) lotypes. Using the more traditional distance-based identifica- Catostomidae 52 10 5 (10) tion approach, we obtained a success rate of 81%. However, the Centrarchidae 32 6 6 (18) inflated proportion of indistinguishable species identified using Cottidae 31 5 6 (16) the distance-based identification approach was mainly caused Ictaluridae 30 0 11 (29) by the presence of cryptic diversity within “known” species. Salmonidae 30 7 0 Thus, approximately half (72 of 141) of the 19% of indistin- Petromyzontidae 27 13 3 (8) fi Fundulidae 26 2 3 (6) guishable species identi ed using the distance-based approach Cichlidae 11 0 0 were those also considered as problematic using the diagnostic Poeciliidae 9 0 0 nucleotide approach. Over half of the remaining problematic Acipenseridae 6 0 0 cases (37 of 69) involved species diverging by over 2% from any Esocidae 5 2 1 (2) other species but were considered as indistinguishable using Gasterosteidae 5 0 1 (2) the distance-based approach because of an even deeper intra- fi Lepisosteidae 5 0 0 speci c divergence (e.g., Nocomis leptocephalus;Fig.1andFig. Clupeidae 4 2 0 S1). For N. leptocephalus, some of the taxa exhibiting deep fi Elassomatidae 4 0 2 (6) intraspeci c divergence values were recovered as poly/para- Embiotocidae 4 0 0 phyletic in phylogenetic trees; nevertheless, all lineages re- Percichthyidae 4 0 0 mained clearly distinct from any other lineages using the Umbridae 4 0 0 diagnostic nucleotide approach and always differed by over 10 Amblyopsidae 3 0 1 (3) characters (e.g., Nocomis spp.; Fig. S1). The lineages
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