Integrative Taxonomy: A Multisource Approach to Exploring Biodiversity
TL;DR: A flexible procedure and stopping rule is presented that uses the information from different disciplines separately for integrative taxonomy, finding that rigor in species delimitation can be increased when several disciplines chosen for complementarity are used.
Abstract: Good alpha taxonomy is central to biology. On the basis of a survey of arthropod studies that used multiple disciplines for species delimitation, we evaluated the performance of single disciplines. All included disciplines had a considerable failure rate. Rigor in species delimitation can thus be increased when several disciplines chosen for complementarity are used. We present a flexible procedure and stopping rule for integrative taxonomy that uses the information from different disciplines separately. Disagreement among disciplines over the number and demarcation of species is resolved by elucidating and invoking evolutionary explanations for disagreement. With the identification of further promising study organisms and of new questions for in-depth analysis, evolutionary biology should profit from integrative taxonomy. An important rationale is clarity in researcher bias in the decision-making process. The success of integrative taxonomy will further increase through methodological progress, taxonomic training of evolutionary biologists, and balanced resource allocation.
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TL;DR: It is concluded that taxonomy needs to be pluralistic to improve species discovery and description, and to develop novel protocols to produce the much-needed inventory of life in a reasonable time.
Abstract: Taxonomy is the biological discipline that identifies, describes, classifies and names extant and extinct species and other taxa. Nowadays, species taxonomy is confronted with the challenge to fully incorporate new theory, methods and data from disciplines that study the origin, limits and evolution of species. Integrative taxonomy has been proposed as a framework to bring together these conceptual and methodological developments. Here we review perspectives for an integrative taxonomy that directly bear on what species are, how they can be discovered, and how much diversity is on Earth. We conclude that taxonomy needs to be pluralistic to improve species discovery and description, and to develop novel protocols to produce the much-needed inventory of life in a reasonable time. To cope with the large number of candidate species revealed by molecular studies of eukaryotes, we propose a classification scheme for those units that will facilitate the subsequent assembly of data sets for the formal description of new species under the Linnaean system, and will ultimately integrate the activities of taxonomists and molecular biologists.
1,389 citations
Cites background from "Integrative Taxonomy: A Multisource..."
...In practice, evidence from all character sets is assembled cumulatively, concordances and discordances are explained from the evolutionary perspective of the populations under study, and a decision is made based on the available information, which can lead to recognition of a species on the basis of a single set of characters if these characters are considered good indicators of lineage divergence (Figure 3b[41,46])....
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...empirical studies support the view that lack of character congruence is a frequent situation [reviewed for arthropods by [41]] resulting from the different modes and circumstances of speciation [e....
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...For example, some taxonomists see congruence among molecular and morphological characters as a necessary requisite [36,40,43] while, for others [23,41,46], the strength of integration lies in avoiding any a priori selection of character combinations....
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...Nonetheless, a general view has emerged that now is the time to construct a more "integrative taxonomy" that would accommodate new concepts and methods [36,37,39-41], and a considerable number of studies have already echoed the new term "integrative taxonomy" [28,31,4245]....
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...However, much of the discussion around integrative taxonomy deals with the merits of morphological versus molecular characters [36-39,41,49]....
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TL;DR: Researchers should apply a wide range of species delimitation analyses to their data and place their trust in delimitations that are congruent across methods, for in most contexts it is better to fail to delimit species than it is to falsely delimit entities that do not represent actual evolutionary lineages.
Abstract: Species delimitation is the act of identifying species-level biological diversity. In recent years, the field has witnessed a dramatic increase in the number of methods available for delimiting species. However, most recent investigations only utilize a handful (i.e. 2–3) of the available methods, often for unstated reasons. Because the parameter space that is potentially relevant to species delimitation far exceeds the parameterization of any existing method, a given method necessarily makes a number of simplifying assumptions, any one of which could be violated in a particular system. We suggest that researchers should apply a wide range of species delimitation analyses to their data and place their trust in delimitations that are congruent across methods. Incongruence across the results from different methods is evidence of either a difference in the power to detect cryptic lineages across one or more of the approaches used to delimit species and could indicate that assumptions of one or more of the methods have been violated. In either case, the inferences drawn from species delimitation studies should be conservative, for in most contexts it is better to fail to delimit species than it is to falsely delimit entities that do not represent actual evolutionary lineages.
918 citations
Cites background from "Integrative Taxonomy: A Multisource..."
...and behaviour (where applicable) of the focal system (Knowles & Carstens 2007; Schlick-Steiner et al. 2010)....
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...This approach is consistent with the spirit of integrative taxonomy, which argues that taxonomic inference should be based on congruence across analyses that utilize multiple sources of data (e.g. Padial et al. 2010; Schlick-Steiner et al. 2010)....
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...…data alone are likely inadequate, and species delimitation should be conducted with consideration of the life history, geographical distribution, morphology © 2013 John Wiley & Sons Ltd and behaviour (where applicable) of the focal system (Knowles & Carstens 2007; Schlick-Steiner et al. 2010)....
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TL;DR: Along with other tools and data types, coalescent-based species delimitation will play an important role in an integrative taxonomy that emphasizes the identification of species limits and the processes that have promoted lineage diversification.
Abstract: The statistical rigor of species delimitation has increased dramatically over the past decade. Coalescent theory provides powerful models for population genetic inference, and is now increasingly important in phylogenetics and speciation research. By applying probabilistic models, coalescent-based species delimitation provides clear and objective testing of alternative hypotheses of evolutionary independence. As acquisition of multilocus data becomes increasingly automated, coalescent-based species delimitation will improve the discovery, resolution, consistency, and stability of the taxonomy of species. Along with other tools and data types, coalescent-based species delimitation will play an important role in an integrative taxonomy that emphasizes the identification of species limits and the processes that have promoted lineage diversification.
727 citations
Agriculture and Agri-Food Canada1, University of Sydney2, Institut national de la recherche agronomique3, Aix-Marseille University4, university of lille5, University of Amsterdam6, American Museum of Natural History7, Leibniz Association8, Ruhr University Bochum9, Universidade Nova de Lisboa10, Federal University of Paraná11, Agro ParisTech12, University of Perugia13, Tuscia University14, Pasteur Institute15, Spanish National Research Council16, Second Military Medical University17, University of Pretoria18, King Abdulaziz University19, Staatliches Museum für Naturkunde Stuttgart20
TL;DR: A novel high fidelity primer pair for TEF1α has potential as a supplementary DNA barcode with superior resolution to ITS, while TOPI and LNS2 are attractive for the Pucciniomycotina, for which universal primers for ribosomal subunits often fail.
Abstract: Primer development and testing by partners in the
European Consortium of Microbial Resource Centres (EMbaRC) was supported
through funding of the European Community’s Seventh Framework
Programme (FP7, 2007–2013), Research Infrastructures action, under grant
agreement no. FP7-228310. Part of sequencing work in CBS was supported
by Fonds Economische Structuurversterking (FES), Dutch Ministry of Education,
Culture and Science grant BEK/BPR-2009/137964-U). WM and VR
were supported by research grant NH&MRC #APP1031952. Genome mining
at CBS and AAFC, and primer development and testing at AAFC, were supported
by grants from the A.P. Sloan Foundation Programme on the Microbiology
of the Built Environment. We acknowledge the Deanship of Scientific
Research (DSR), King Abdulaziz University, under grant No. 1-965/1434 HiCi
for technical and financial support. AY was supported by Fundacao para a
Ciencia e a Tecnologia (Portugal), project PTDC/BIA-BIC/4585/2012. MPM
was supported by grant CGL2012-359 (Spain).
385 citations
Cites background from "Integrative Taxonomy: A Multisource..."
...An intense debate is ongoing concerning whether the identification of organisms of unresolved alpha taxonomy is amenable to DNA barcoding, because in silico-based identi fication requires gene sequences that accurately reflect natural classifications (Eberhardt 2010, Schlick-Steiner et al. 2010)....
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TL;DR: It is time for incorporating multicriteria species approaches aiming to understand speciation across space and taxa, thus allowing integration into biodiversity conservation while accommodating for species uncertainty.
Abstract: The species concept is the cornerstone of biodiversity science, and any paradigm shift in the delimitation of species affects many research fields. Many biologists now are embracing a new "species" paradigm as separately evolving populations using different delimitation criteria. Individual criteria can emerge during different periods of speciation; some may never evolve. As such, a paradigm shift in the species concept relates to this inherent heterogeneity in the speciation process and species category-which is fundamentally overlooked in biodiversity research. Cryptic species fall within this paradigm shift: they are continuously being reported from diverse animal phyla but are poorly considered in current tests of ecological and evolutionary theory. The aim of this review is to integrate cryptic species in biodiversity science. In the first section, we address that the absence of morphological diversification is an evolutionary phenomenon, a "process" counterpart to the long-studied mechanisms of morphological diversification. In the next section regarding taxonomy, we show that molecular delimitation of cryptic species is heavily biased towards distance-based methods. We also stress the importance of formally naming of cryptic species for better integration into research fields that use species as units of analysis. Finally, we show that incorporating cryptic species leads to novel insights regarding biodiversity patterns and processes, including large-scale biodiversity assessments, geographic variation in species distribution and species coexistence. It is time for incorporating multicriteria species approaches aiming to understand speciation across space and taxa, thus allowing integration into biodiversity conservation while accommodating for species uncertainty.
334 citations
Cites background from "Integrative Taxonomy: A Multisource..."
...It can either provide additional support for a species hypothesis (Schlick-Steiner et al., 2010) or detect contradictions among data (Padial et al., 2010); both help link taxonomy with evolutionary biology (Sites & Marshall, 2003, 2004)....
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...Finding morphological diagnostic traits among morphologically cryptic species is challenging (Fi ser & Zagmajster, 2009; Schlick-Steiner et al., 2010) and the practical value of such diagnoses may be questionable (Jugovic et al., 2012)....
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References
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Book•
01 Jan 1989
6,659 citations
"Integrative Taxonomy: A Multisource..." refers background in this paper
..., a taxonomic construct assigned to the species category, is a hypothesis and should not be seen as true even if well-supported (47)....
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TL;DR: A simple approach for accounting for genotypic ambiguity in studies of population structure and apply it to AFLP data from whitefish is presented.
Abstract: Dominant markers such as amplified fragment length polymorphisms (AFLPs) provide an economical way of surveying variation at many loci. However, the uncertainty about the underlying genotypes presents a problem for statistical analysis. Similarly, the presence of null alleles and the limitations of genotype calling in polyploids mean that many conventional analysis methods are invalid for many organisms. Here we present a simple approach for accounting for genotypic ambiguity in studies of population structure and apply it to AFLP data from whitefish. The approach is implemented in the program structure version 2.2, which is available from http://pritch.bsd.uchicago.edu/structure.html.
4,274 citations
"Integrative Taxonomy: A Multisource..." refers background or methods in this paper
...Such methods are standard procedure for some disciplines, such as in DNA-based phylogenetic reconstruction (17), and are also available for population genetics analysis (16)....
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...An example would be to subject population genetics data to cluster analysis (16)....
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TL;DR: This work uses computer simulations and a laboratory-generated phylogeny to test bootstrapping results of parsimony analyses, and indicates that any given bootstrap proportion provides an unbiased but highly imprecise measure of repeatability, unless the actual probability of replicating the relevant result is nearly one.
Abstract: Bootstrapping is a common method for assessing confidence in phylogenetic anal? yses. Although bootstrapping was first applied in phylogenetics to assess the repeatability of a given result, bootstrap results are commonly interpreted as a measure of the probability that a phylogenetic estimate represents the true phylogeny. Here we use computer simulations and a laboratory-generated phylogeny to test bootstrapping results of parsimony analyses, both as measures of repeatability (i.e., the probability of repeating a result given a new sample of characters) and accuracy (i.e., the probability that a result represents the true phylogeny). Our results indicate that any given bootstrap proportion provides an unbiased but highly imprecise measure of repeatability, unless the actual probability of replicating the relevant result is nearly one. The imprecision of the estimate is great enough to render the estimate virtually useless as a measure of repeatability. Under conditions thought to be typical of most phylogenetic analyses, however, bootstrap proportions in majority-rule consensus trees provide biased but highly con? servative estimates of the probability of correctly inferring the corresponding clades. Specifically, under conditions of equal rates of change, symmetric phylogenies, and internodal change of 70% usually correspond to a probability of >95% that the corresponding dade is real. However, under conditions of very high rates of internodal change (approaching randomization of the characters among taxa) or highly unequal rates of change among taxa, bootstrap proportions >50% are overestimates of accuracy. (Boot? strapping; accuracy; repeatability; phylogeny; parsimony; precision; statistical analyses; simu? lations.)
4,057 citations
"Integrative Taxonomy: A Multisource..." refers methods in this paper
...For considering clades in phylogenetic reconstructions as significantly supported, we applied a cut-off value for node support of >70 to bootstrapping results (26) and >0....
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TL;DR: A unified species concept can be achieved by treating existence as a separately evolving metapopulation lineage as the only necessary property of species and the former secondary species criteria as different lines of evidence relevant to assessing lineage separation.
Abstract: The issue of species delimitation has long been confused with that of species conceptualization, leading to a half century of controversy concerning both the definition of the species category and methods for inferring the boundaries and numbers of species. Alternative species concepts agree in treating existence as a separately evolving metapopulation lineage as the primary defining property of the species category, but they disagree in adopting different properties acquired by lineages during the course of divergence (e.g., intrinsic reproductive isolation, diagnosability, monophyly) as secondary defining properties (secondary species criteria). A unified species concept can be achieved by treating existence as a separately evolving metapopulation lineage as the only necessary property of species and the former secondary species criteria as different lines of evidence (operational criteria) relevant to assessing lineage separation. This unified concept of species has several consequences for species delimitation, including the following: First, the issues of species conceptualization and species delimitation are clearly separated; the former secondary species criteria are no longer considered relevant to species conceptualization but only to species delimitation. Second, all of the properties formerly treated as secondary species criteria are relevant to species delimitation to the extent that they provide evidence of lineage separation. Third, the presence of any one of the properties (if appropriately interpreted) is evidence for the existence of a species, though more properties and thus more lines of evidence are associated with a higher degree of corroboration. Fourth, and perhaps most significantly, a unified species concept shifts emphasis away from the traditional species criteria, encouraging biologists to develop new methods of species delimitation that are not tied to those properties.
2,875 citations
TL;DR: The literature on cryptic and sibling species is synthesized and trends in their discovery are discussed, suggesting that the discovery of cryptic species is likely to be non-random with regard to taxon and biome and could have profound implications for evolutionary theory, biogeography and conservation planning.
Abstract: The taxonomic challenge posed by cryptic species (two or more distinct species classified as a single species) has been recognized for nearly 300 years, but the advent of relatively inexpensive and rapid DNA sequencing has given biologists a new tool for detecting and differentiating morphologically similar species. Here, we synthesize the literature on cryptic and sibling species and discuss trends in their discovery. However, a lack of systematic studies leaves many questions open, such as whether cryptic species are more common in particular habitats, latitudes or taxonomic groups. The discovery of cryptic species is likely to be non-random with regard to taxon and biome and, hence, could have profound implications for evolutionary theory, biogeography and conservation planning.
2,837 citations