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The unholy trinity: Taxonomy, species delimitation and DNA barcoding

The Royal Society
Philosophical Transactions B
Authors:
Robert Desalle at American Museum of Natural History
Robert Desalle
Mary G Egan
Mary G Egan
Mary G Egan
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Mark Siddall
Mark Siddall
Mark Siddall
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Abstract

Recent excitement over the development of an initiative to generate DNA sequences for all named species on the planet has in our opinion generated two major areas of contention as to how this 'DNA barcoding' initiative should proceed. It is critical that these two issues are clarified and resolved, before the use of DNA as a tool for taxonomy and species delimitation can be universalized. The first issue concerns how DNA data are to be used in the context of this initiative; this is the DNA barcode reader problem (or barcoder problem). Currently, many of the published studies under this initiative have used tree building methods and more precisely distance approaches to the construction of the trees that are used to place certain DNA sequences into a taxonomic context. The second problem involves the reaction of the taxonomic community to the directives of the 'DNA barcoding' initiative. This issue is extremely important in that the classical taxonomic approach and the DNA approach will need to be reconciled in order for the 'DNA barcoding' initiative to proceed with any kind of community acceptance. In fact, we feel that DNA barcoding is a misnomer. Our preference is for the title of the London meetings--Barcoding Life. In this paper we discuss these two concerns generated around the DNA barcoding initiative and attempt to present a phylogenetic systematic framework for an improved barcoder as well as a taxonomic framework for interweaving classical taxonomy with the goals of 'DNA barcoding'.
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The unholy trinity: taxonomy, species delimitation
and DNA barcoding
Rob DeSalle*, Mary G. Egan and Mark Siddall
Division of Invertebrate Zoology, American Museum of Natural History, 79th Street at Central Park West,
New York, NY 10024, USA
Recent excitement over the development of an initiative to generate DNA sequences for all named
species on the planet has in our opinion generated two major areas of contention as to how this ‘DNA
barcoding’ initiative should proceed. It is critical that these two issues are clarified and resolved,
before the use of DNA as a tool for taxonomy and species delimitation can be universalized. The first
issue concerns how DNA data are to be used in the context of this initiative; this is the DNA barcode
reader problem (or barcoder problem). Currently, many of the published studies under this initiative
have used tree building methods and more precisely distance approaches to the construction of the
trees that are used to place certain DNA sequences into a taxonomic context. The second problem
involves the reaction of the taxonomic community to the directives of the ‘DNA barcoding’ initiative.
This issue is extremely important in that the classical taxonomic approach and the DNA approach
will need to be reconciled in order for the ‘DNA barcoding’ initiative to proceed with any kind of
community acceptance. In fact, we feel that DNA barcoding is a misnomer. Our preference is for the
title of the London meetings—Barcoding Life. In this paper we discuss these two concerns generated
around the DNA barcoding initiative and attempt to present a phylogenetic systematic framework for
an improved barcoder as well as a taxonomic framework for interweaving classical taxonomy with the
goals of ‘DNA barcoding’.
Keywords: DNA barcoding; taxonomy; species delimitation; muntjac; leeches; sturgeon
1. INTRODUCTION: BUILDING A BETTER DNA
BARCODER
One of the major issues concerning the inclusion of
molecular information into taxonomic aspects of
biology that has yet to be discussed in detail in the
commentaries on this subject is concerning the best
way to read the barcodes. There are two separate tasks
to which DNA barcodes are currently being applied.
The first is the use of DNA data to distinguish between
species (equivalent to species identification or species
diagnosis) and the second is the use of DNA data to
discover new species (equivalent to species delimita-
tion, species description). These two activities differ in
the types and amount of data required. Below we
highlight some of the issues that may limit the utility of
current DNA barcoding endeavours (especially those
used for species discovery) and suggest a framework for
the development of a barcoder that addresses these
issues.
(a)The barcoder engine: distances or characters?
A major issue that needs to be resolved is how to read
the organismal barcode once it is generated. Most
recently published approaches to DNA barcoding have
utilized distance measures to make the inference as to
species designation (Hebert et al. 2003a,b,2004a,b).
Distances are used in two major approaches; the first is
a simple BLAST (Altschul et al. 1990) approach where
a raw similarity score is used to determine the nearest
neighbour to the query sequence. The second
approach utilizes distances in tree building (Hebert
et al. 2003a,b). We point out the following short-
comings with these approaches and further suggest that
character based approaches are more appropriate for
DNA barcoding both for theoretical and for practical
reasons.
A major shortcoming of using distances in DNA
barcoding is that all classical studies and taxonomic
schemes that accomplish the same thing that barcodes
are meant to accomplish are character based, making
the union of classical and DNA barcoding a difficult
process if the use of distances is continued in barcoding
studies (see below). This shortcoming also is related to
the need for diagnostic characters that classical studies
use to validate the existence of a species. A second
shortcoming is that similarity scores often do not give
the nearest neighbour as the closest relative (Koski &
Golding 2001). Nevertheless, similarity scores will
always give a nearest neighbour. Character based
methods have the logical advantage that when diag-
nostic character data are lacking, they will fail to
diagnose, allowing for a degree of hypothesis testing not
available when using distances. A third shortcoming
involves the lack of an objective set of criteria to
delineate taxa when using distances. For example, a
universal similarity cut-off to determine species status
will simply not exist, because of the broad overlap of
inter- and intra-specific distances (Goldstein et al.
2000). Researchers will have to constantly revise their
similarity cut-offs from group to group. We suspect that
Phil. Trans. R. Soc. B (2005) 360, 1905–1916
doi:10.1098/rstb.2005.1722
Published online 14 September 2005
One contribution of 18 to a Theme Issue ‘DNA barcoding of life’.
*Author for correspondence (desalle@amnh.org).
1905 q2005 The Royal Society
... Obviously, the analysis of DNA sequences provides very powerful lines of taxonomic evidence, leading even to proposals of purely DNA-based taxonomy [27]. Indeed, although DNA barcoding was mostly conceived for specimen identification, its application was rapidly extended to also encompass species discovery and delimitation [28][29][30][31]. Organellar DNA sequences such as COI barcodes represent the majority of the molecular data produced so far by taxonomists, as they are easy to amplify and remarkably informative due to their high evolutionary rate. ...
... Considering a probabilistic approach to species, this basically means that the lower the genetic distance of a subset Fig. 6 Three different previously published workflows of integrative species delimitation. (a) The "taxonomic circle" (from DeSalle et al. [29]). This protocol represents the congruence approach proposed by these authors. ...
... The biogeographical context constitutes an important interpretative framework. Interestingly, many species delimitation approaches invoke allopatry, i.e., absence of co-occurrence, as a relevant criterion to consider two genetically divergent subsets as distinct species [16,29]. In contrast, along with Hillis et al. [83], we highlight that co-occurrence of two subsets of individuals without admixture in sympatry or parapatry provides the ultimate evidence for them representing two distinct species and thus highly valuable information in species delimitation. ...
DNA Barcoding in Species Delimitation: From Genetic Distances to Integrative Taxonomy
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Over the past two decades, DNA barcoding has become the most popular exploration approach in molecular taxonomy, whether for identification, discovery, delimitation, or description of species. The present contribution focuses on the utility of DNA barcoding for taxonomic research activities related to species delimitation, emphasizing the following aspects: (1) To what extent DNA barcoding can be a valuable ally for fundamental taxonomic research, (2) its methodological and theoretical limitations, (3) the conceptual background and practical use of pairwise distances between DNA barcode sequences in taxonomy, and (4) the different ways in which DNA barcoding can be combined with complementary means of investigation within a broader integrative framework. In this chapter, we recall and discuss the key conceptual advances that have led to the so-called renaissance of taxonomy, elaborate a detailed glossary for the terms specific to this discipline (see Glossary in Chap. 35), and propose a newly designed step-by-step species delimitation protocol starting from DNA barcode data that includes steps from the preliminary elaboration of an optimal sampling strategy to the final decision-making process which potentially leads to nomenclatural changes.
View
... In biological groups where the traditional taxonomy is ambiguous or where speciation has occurred without changes in morphological features, molecular data is an important tool for delimiting species (Hebert et al. 2003 a,b;Hebert et al. 2004;Barrett & Hebert 2005). Using an integrative approach that corroborates hypotheses generated from multiple approaches and under different lines of evidence is essential, with species limits expected to show congruency across all results (DeSalle et al. 2005;Carstens et al. 2013). ...
... These methods and approximations can differ amongst themselves and often show results that depend on the study group Valdez-Mondragón 2020;Nolasco & Valdez-Mondragón 2022). Therefore, it is recommended to use more than one molecular method to define more precise species hypotheses, in combination with morphological evidence as part of an integrative approach (Dayrat 2005;DeSalle et al. 2005;Padial et al. 2010;Carstens et al. 2013). ...
Violins we see, species we don’t… Species delimitation of the spider genus Loxosceles Heineken & Lowe (Araneae: Sicariidae) from North America using morphological and molecular evidence
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... DNA taxonomy 1 -to characterize species based on DNA sequences-has become well feasible and highly effective in the past two decades [1][2][3][4]. Meanwhile, the array and number of markers (Table 1) and approaches for species identification and delimitation have considerably diversified [5][6][7]. ...
Species Diagnosis and DNA Taxonomy
Article
  • Apr 2024
The use of DNA has helped to improve and speed up species identification and delimitation. However, it also provides new challenges to taxonomists. Incongruence of outcome from various markers and delimitation methods, bias from sampling and skewed species distribution, implemented models, and the choice of methods/priors may mislead results and also may, in conclusion, increase elements of subjectivity in species taxonomy. The lack of direct diagnostic outcome from most contemporary molecular delimitation approaches and the need for a reference to existing and best sampled trait reference systems reveal the need for refining the criteria of species diagnosis and diagnosability in the current framework of nomenclature codes and good practices to avoid nomenclatorial instability, parallel taxonomies, and consequently more and new taxonomic impediment.
View
... Because it is not always feasible to discriminate between species belonging to the same genus, larval taxonomy is complex and time-consuming " (Burington, 2011;Ruiter et al., 2013)." "By permitting fast surveys of novel regions, In combination with traditional taxonomy, DNA barcoding and the use of sequence databases can help speed up this process (Ruiter et al., 2013;DeSalle, Egan and Siddall, 2005;Jinbo et al., 2011;Pauls et al., 2010;Zhou et al., 2007). The Barcode of Life Database (BOLD) contains DNA barcodes for approximately 260,000 species, including 4555 Trichoptera species, and enables species identification using the COI DNA gene component I (Mir et al., 2020)." ...
Generating The DNA Barcodes of Indian Caddisflies (Tricoptera: Insecta): A Way Forward
Chapter
  • Apr 2024
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View
... Because it is not always feasible to discriminate between species belonging to the same genus, larval taxonomy is complex and time-consuming " (Burington, 2011;Ruiter et al., 2013)." "By permitting fast surveys of novel regions, In combination with traditional taxonomy, DNA barcoding and the use of sequence databases can help speed up this process (Ruiter et al., 2013;DeSalle, Egan and Siddall, 2005;Jinbo et al., 2011;Pauls et al., 2010;Zhou et al., 2007). The Barcode of Life Database (BOLD) contains DNA barcodes for approximately 260,000 species, including 4555 Trichoptera species, and enables species identification using the COI DNA gene component I (Mir et al., 2020)." ...
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Full-text available
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View
... Because it is not always feasible to discriminate between species belonging to the same genus, larval taxonomy is complex and time-consuming " (Burington, 2011;Ruiter et al., 2013)." "By permitting fast surveys of novel regions, In combination with traditional taxonomy, DNA barcoding and the use of sequence databases can help speed up this process (Ruiter et al., 2013;DeSalle, Egan and Siddall, 2005;Jinbo et al., 2011;Pauls et al., 2010;Zhou et al., 2007). The Barcode of Life Database (BOLD) contains DNA barcodes for approximately 260,000 species, including 4555 Trichoptera species, and enables species identification using the COI DNA gene component I (Mir et al., 2020)." ...
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