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      Response to Zamani et al. (2020): The omission of critical data in the pursuit of “revolutionary” methods to accelerate the description of species

      , 1 , 2 , 3 , 4

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          Abstract

          Here we respond to the criticisms leveled against a proposal that suggested an efficient solution to the taxonomic impediment. We clarify some of our objectives and demonstrate that many of the criticisms apply more to traditional approaches to taxonomy rather than to our minimalist approach.

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          Most cited references 24

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          A DNA-Based Registry for All Animal Species: The Barcode Index Number (BIN) System

          Because many animal species are undescribed, and because the identification of known species is often difficult, interim taxonomic nomenclature has often been used in biodiversity analysis. By assigning individuals to presumptive species, called operational taxonomic units (OTUs), these systems speed investigations into the patterning of biodiversity and enable studies that would otherwise be impossible. Although OTUs have conventionally been separated through their morphological divergence, DNA-based delineations are not only feasible, but have important advantages. OTU designation can be automated, data can be readily archived, and results can be easily compared among investigations. This study exploits these attributes to develop a persistent, species-level taxonomic registry for the animal kingdom based on the analysis of patterns of nucleotide variation in the barcode region of the cytochrome c oxidase I (COI) gene. It begins by examining the correspondence between groups of specimens identified to a species through prior taxonomic work and those inferred from the analysis of COI sequence variation using one new (RESL) and four established (ABGD, CROP, GMYC, jMOTU) algorithms. It subsequently describes the implementation, and structural attributes of the Barcode Index Number (BIN) system. Aside from a pragmatic role in biodiversity assessments, BINs will aid revisionary taxonomy by flagging possible cases of synonymy, and by collating geographical information, descriptive metadata, and images for specimens that are likely to belong to the same species, even if it is undescribed. More than 274,000 BIN web pages are now available, creating a biodiversity resource that is positioned for rapid growth.
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            Counting animal species with DNA barcodes: Canadian insects

            Recent estimates suggest that the global insect fauna includes fewer than six million species, but this projection is very uncertain because taxonomic work has been limited on some highly diverse groups. Validation of current estimates minimally requires the investigation of all lineages that are diverse enough to have a substantial impact on the final species count. This study represents a first step in this direction; it employs DNA barcoding to evaluate patterns of species richness in 27 orders of Canadian insects. The analysis of over one million specimens revealed species counts congruent with earlier results for most orders. However, Diptera and Hymenoptera were unexpectedly diverse, representing two-thirds of the 46 937 barcode index numbers (=species) detected. Correspondence checks between known species and barcoded taxa showed that sampling was incomplete, a result confirmed by extrapolations from the barcode results which suggest the occurrence of at least 94 000 species of insects in Canada, a near doubling from the prior estimate of 54 000 species. One dipteran family, the Cecidomyiidae, was extraordinarily diverse with an estimated 16 000 species, a 10-fold increase from its predicted diversity. If Canada possesses about 1% of the global fauna, as it does for known taxa, the results of this study suggest the presence of 10 million insect species with about 1.8 million of these taxa in the Cecidomyiidae. If so, the global species count for this fly family may exceed the combined total for all 142 beetle families. If extended to more geographical regions and to all hyperdiverse groups, DNA barcoding can rapidly resolve the current uncertainty surrounding a species count for the animal kingdom. A newly detailed understanding of species diversity may illuminate processes important in speciation, as suggested by the discovery that the most diverse insect lineages in Canada employ an unusual mode of reproduction, haplodiploidy. This article is part of the themed issue ‘From DNA barcodes to biomes’.
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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 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, non-monophyly 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 non-monophyly in COI (a.k.a. cox1) 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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                Author and article information

                Contributors
                Role: ConceptualizationRole: InvestigationRole: VisualizationRole: Writing - original draft
                Journal
                Zookeys
                Zookeys
                2
                urn:lsid:arphahub.com:pub:45048D35-BB1D-5CE8-9668-537E44BD4C7E
                urn:lsid:zoobank.org:pub:91BD42D4-90F1-4B45-9350-EEF175B1727A
                ZooKeys
                Pensoft Publishers
                1313-2989
                1313-2970
                2021
                22 April 2021
                : 1033
                : 191-201
                Affiliations
                [1 ] The Hymenoptera Institute, 116 Franklin Ave., Redlands, CA 92373, USA The Hymenoptera Institute Redlands United States of America
                [2 ] Entomology Section, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, CA 90007, USA Natural History Museum of Los Angeles County Los Angeles United States of America
                [3 ] Department of Entomology, University of California, Riverside, CA, USA University of California Riverside United States of America
                [4 ] Ecology and Genetics Research Unit, University of Oulu, Finland University of Oulu Oulu Finland
                Author notes
                Corresponding author: Michael Sharkey ( msharkey@ 123456uky.edu )

                Academic editor: Lyubomir Penev

                Article
                66186
                10.3897/zookeys.1033.66186
                8084859
                33958926
                Michael Sharkey, Brian Brown, Austin Baker, Marko Mutanen

                This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Categories
                Editorial
                Animalia
                Braconidae
                Biodiversity & Conservation
                Systematics
                Americas
                Central America and the Caribbean
                World

                Animal science & Zoology

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