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      Species delimitation based on diagnosis and monophyly, and its importance for advancing mammalian taxonomy

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          Abstract

          A recently proposed taxonomic classification of extant ungulates sparked a series of publications that criticize the Phylogenetic Species Concept (PSC) claiming it to be a particularly poor species concept. These opinions reiteratively stated that (1) the two fundamental elements of the "PSC", i.e., monophyly and diagnosability, do not offer objective criteria as to where the line between species should be drawn; and (2) that extirpation of populations can lead to artificial diagnosability and spurious recognitions of species. This sudden eruption of criticism against the PSC is misleading. Problems attributed to the PSC are common to most approaches and concepts that modern systematists employ to establish species boundaries. The controversial taxonomic propositions that sparked criticism against the PSC are indeed highly problematic, not because of the species concept upon which they are based, but because no evidence (whatsoever) has become public to support a substantial portion of the proposed classification. We herein discuss these topics using examples from mammals. Numerous areas of biological research rest upon taxonomic accuracy (including conservation biology and biomedical research); hence, it is necessary to clarify what are (and what are not) the real sources of taxonomic inaccuracy.

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          Gene Trees in Species Trees

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            Taxonomic inflation: its influence on macroecology and conservation.

            Species numbers are increasing rapidly. This is due mostly to taxonomic inflation, where known subspecies are raised to species as a result in a change in species concept, rather than to new discoveries. Yet macroecologists and conservation biologists depend heavily on species lists, treating them as accurate and stable measures of biodiversity. Deciding on a standardized, universal species list might ameliorate the mismatch between taxonomy and the uses to which it is put. However, taxonomic uncertainty is ultimately due to the evolutionary nature of species, and is unlikely to be solved completely by standardization. For the moment, at least, users must acknowledge the limitations of taxonomic species and avoid unrealistic expectations of species lists.
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              Delimiting species without monophyletic gene trees.

              Genetic data are frequently used to delimit species, where species status is determined on the basis of an exclusivity criterium, such as reciprocal monophyly. Not only are there numerous empirical examples of incongruence between the boundaries inferred from such data compared to other sources like morphology -- especially with recently derived species, but population genetic theory also clearly shows that an inevitable bias in species status results because genetic thresholds do not explicitly take into account how the timing of speciation influences patterns of genetic differentiation. This study represents a fundamental shift in how genetic data might be used to delimit species. Rather than equating gene trees with a species tree or basing species status on some genetic threshold, the relationship between the gene trees and the species history is modeled probabilistically. Here we show that the same theory that is used to calculate the probability of reciprocal monophyly can also be used to delimit species despite widespread incomplete lineage sorting. The results from a preliminary simulation study suggest that very recently derived species can be accurately identified long before the requisite time for reciprocal monophyly to be achieved following speciation. The study also indicates the importance of sampling, both with regards to loci and individuals. Withstanding a thorough investigation into the conditions under which the coalescent-based approach will be effective, namely how the timing of divergence relative to the effective population size of species affects accurate species delimitation, the results are nevertheless consistent with other recent studies (aimed at inferring species relationships), showing that despite the lack of monophyletic gene trees, a signal of species divergence persists and can be extracted. Using an explicit model-based approach also avoids two primary problems with species delimitation that result when genetic thresholds are applied with genetic data -- the inherent biases in species detection arising from when and how speciation occurred, and failure to take into account the high stochastic variance of genetic processes. Both the utility and sensitivities of the coalescent-based approach outlined here are discussed; most notably, a model-based approach is essential for determining whether incompletely sorted gene lineages are (or are not) consistent with separate species lineages, and such inferences require accurate model parameterization (i.e., a range of realistic effective population sizes relative to potential times of divergence for the purported species). It is the goal (and motivation of this study) that genetic data might be used effectively as a source of complementation to other sources of data for diagnosing species, as opposed to the exclusion of other evidence for species delimitation, which will require an explicit consideration of the effects of the temporal dynamic of lineage splitting on genetic data.
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                Author and article information

                Journal
                Zool Res
                Zool Res
                Zoological Research
                Science Press (16 Donghuangchenggen Beijie, Beijing 100717, China )
                2095-8137
                08 March 2018
                18 September 2018
                : 39
                : 5
                : 301-308
                Affiliations
                [1 ]Pós-Graduação em Biodiversidade Animal, Departamento de Ecologia e Evolução, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Santa Maria, RS 97105-900, Brazil
                [2 ]Division of Mammals, National Museum of Natural History, Smithsonian Institution, Washington DC 20013-7012, USA
                [3 ]Pós-graduação, Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais 31270-901, Brazil
                Author notes
                [* ]Corresponding author, E-mail: ee.gutierrez.bio@ 123456gmail.com
                Article
                ZoolRes-39-5-301
                10.24272/j.issn.2095-8137.2018.037
                6102684
                29551763
                1aaeae8d-4e3c-4301-a07a-15ac3ed79942
                © 2018. Editorial Office of Zoological Research, Kunming Institute of Zoology, Chinese Academy of Sciences

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

                History
                : 14 December 2017
                : 12 February 2018
                Categories
                Article

                alpha taxonomy,phylogenetic species concept,species concepts,taxonomic inertia,taxonomic inflation

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