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      Poly-paraphyly of Hirudinidae: many lineages of medicinal leeches

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      BMC Evolutionary Biology
      BioMed Central

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          Abstract

          Background

          Medicinal leeches became infamous for their utility in bloodletting popularized in the 19 th century, and have seen a recent resurgence in post-operative treatments for flap and replantation surgeries, and in terms of characterization of salivary anticoagulants. Notorious throughout the world, the quintessential leech family Hirudinidae has been taken for granted to be monophyletic, as has the non-bloodfeeding family Haemopidae.

          Results

          This study is the first to evaluate molecular evidence from hirudinid and haemopid leeches in a manner that encompasses the global scope of their taxonomic distributions. We evaluated the presumed monophyly of the Hirudinidae and assessed previous well-accepted classification schemes. The Hirudinidae were found not to be monophyletic, falling instead into two distinct and unrelated clades. Members of the non-bloodfeeding family Haemopidae were scattered throughout the tree and among traditional hirudinid genera. A combination of nuclear 18S rDNA and 28S rDNA with mitochondrial 12S rDNA and cytochrome c oxidase I were analyzed with Parsimony and with Bayesian methods.

          Conclusion

          The family Hirudinidae must be refined to include only the clade containing Hirudo medicinalis (European medicinal leech) and related leeches irrespective of bloodfeeding behavior. A second clade containing Macrobdella decora (North American medicinal leech) and its relatives may yet be recognized in Semiscolecidae in order to avoid paraphyly. The African distribution of species from each of the divergent hirudinid clades suggests that a deep divergence took place in the history of the medicinal leeches hundreds of millions of years ago.

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          Most cited references39

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          Phylogenetic Inference From Restriction Endonuclease Cleavage Site Maps with Particular Reference to the Evolution of Humans and the Apes

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            The importance of data partitioning and the utility of Bayes factors in Bayesian phylogenetics.

            As larger, more complex data sets are being used to infer phylogenies, accuracy of these phylogenies increasingly requires models of evolution that accommodate heterogeneity in the processes of molecular evolution. We investigated the effect of improper data partitioning on phylogenetic accuracy, as well as the type I error rate and sensitivity of Bayes factors, a commonly used method for choosing among different partitioning strategies in Bayesian analyses. We also used Bayes factors to test empirical data for the need to divide data in a manner that has no expected biological meaning. Posterior probability estimates are misleading when an incorrect partitioning strategy is assumed. The error was greatest when the assumed model was underpartitioned. These results suggest that model partitioning is important for large data sets. Bayes factors performed well, giving a 5% type I error rate, which is remarkably consistent with standard frequentist hypothesis tests. The sensitivity of Bayes factors was found to be quite high when the across-class model heterogeneity reflected that of empirical data. These results suggest that Bayes factors represent a robust method of choosing among partitioning strategies. Lastly, results of tests for the inclusion of unexpected divisions in empirical data mirrored the simulation results, although the outcome of such tests is highly dependent on accounting for rate variation among classes. We conclude by discussing other approaches for partitioning data, as well as other applications of Bayes factors.
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              Higher level relationships of leeches (Annelida: Clitellata: Euhirudinea) based on morphology and gene sequences.

              The evolutionary patterns of divergence of seven euhirudinean families were investigated by cladistic analysis of 33 euhirudinean species. Oligochaetes, Acanthobdella peledina, and branchiobdellidans were included as outgroup taxa. Cladistic analysis employed 1.8 kb of nuclear 18S ribosomal DNA and 651 bp of mitochondrial cytochrome c oxidase subunit I in addition to morphological data. The use of two molecular data sets, one nuclear gene and one mitochondrial gene, as well as morphological data combined historical information evolving under a variety of different constraints and therefore was less susceptible to the biases that could confound the use of only one type of data. Results suggest that the nuclear 18S rDNA gene yields a meaningful historical signal for determining higher level relationships. The more rapidly evolving CO-I gene was informative for recent or local areas of the evolutionary hypothesis, such as within-family relationships. Analyses combining all data from the three character sets yielded one most-parsimonious tree. Most of the higher taxa in recent leech systematics were well corroborated in the resulting topology. However, these results suggested paraphyly of the order Rhynchobdellida, which contradicts the presence of a proboscis as a synapomorphy. The medicinal leech family Hirudinidae was polyphyletic because Haemadipsidae and Haemopidae each have a hirudinid ancestor. In addition, all but one of the genera within the family Erpobdellidae must be either abandoned or renamed. Unusual findings included compelling evidence of historical plasticity in bloodfeeding behavior, having been lost at least four times in the course of euhirudinean evolution. Biogeographic patterns supported a New World origin for Arhynchobdellida. Copyright 1999 Academic Press.
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                Author and article information

                Journal
                BMC Evol Biol
                BMC Evolutionary Biology
                BioMed Central
                1471-2148
                2009
                7 October 2009
                : 9
                : 246
                Affiliations
                [1 ]Department of Biology, The Graduate Center, The City University of New York, New York, NY, USA
                [2 ]Division of Invertebrate Zoology, American Museum of Natural History, New York, NY, USA
                Article
                1471-2148-9-246
                10.1186/1471-2148-9-246
                2768714
                19811660
                943fdc5a-49a9-4c4b-b073-2118031c01f0
                Copyright © 2009 Phillips and Siddall; licensee BioMed Central Ltd.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 2 April 2009
                : 7 October 2009
                Categories
                Research Article

                Evolutionary Biology
                Evolutionary Biology

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