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      Multiple gene analyses of caligid copepods indicate that the reduction of a thoracic appendage in Pseudocaligus represents convergent evolution

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          Abstract

          Background

          The Caligidae is a family of parasitic copepods containing over 30 recognised genera. They are commercially important parasites as they cause disease in numerous finfish aquaculture facilities globally. Morphological features are used to distinguish between the genera and Pseudocaligus has traditionally been differentiated from Caligus solely by the presence of a much reduced form of the fourth thoracic leg. Currently there are numerous DNA sequences available for Caligus spp. but only the type species, Pseudocaligus brevipedis, has molecular data available, so systematic studies using molecular phylogenetic analyses have been limited.

          Methods

          Three gene regions, SSU rDNA, 16S and CO1, for Pseudocaligus fugu from puffer fish from Japan and Pseudocaligus uniartus from rabbit fish from Indonesia are sequenced and molecular phylogenetic analyses performed in order to infer phylogenetic relationships between Pseudocaligus and other caligid copepods.

          Results

          The analysis revealed that there was no discrete grouping of Pseudocaligus spp. and that they had a polyphyletic distribution within Caligus taxa. Pseudocaligus fugu grouped with Caligus elongatus and contained a unique synapomorphy in the SSU rDNA region only seen in members of that clade. Pseudocaligus uniartus formed a well-supported group, in the SSU rDNA analyses, with a Caligus sp. that also infects rabbit fish, but was unresolved in the other analyses. Pseudocaligus brevipedis consistently and robustly grouped with Caligus curtus and C. centrodonti in all analyses. The majority of Lepeophtheirus spp. form a monophyletic sister group to the Caligus clade; however, L. natalensis is unresolved in all analyses and does not form part of the main Lepeophtheirus clade.

          Conclusions

          These findings do not support the morphological-based distinction between Pseudocaligus and Caligus, suggesting that the reduced fourth leg is a feature that has evolved on multiple occasions throughout caligid evolution. Congruent molecular phylogenetic data support groupings based on the presence of morphological features, such as lunules, geography and host fish type rather than appendage morphology. Therefore, we support the synonymy of Pseudocaligus with Caligus.

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          Most cited references19

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          Bayesian phylogenetic analysis of combined data.

          The recent development of Bayesian phylogenetic inference using Markov chain Monte Carlo (MCMC) techniques has facilitated the exploration of parameter-rich evolutionary models. At the same time, stochastic models have become more realistic (and complex) and have been extended to new types of data, such as morphology. Based on this foundation, we developed a Bayesian MCMC approach to the analysis of combined data sets and explored its utility in inferring relationships among gall wasps based on data from morphology and four genes (nuclear and mitochondrial, ribosomal and protein coding). Examined models range in complexity from those recognizing only a morphological and a molecular partition to those having complex substitution models with independent parameters for each gene. Bayesian MCMC analysis deals efficiently with complex models: convergence occurs faster and more predictably for complex models, mixing is adequate for all parameters even under very complex models, and the parameter update cycle is virtually unaffected by model partitioning across sites. Morphology contributed only 5% of the characters in the data set but nevertheless influenced the combined-data tree, supporting the utility of morphological data in multigene analyses. We used Bayesian criteria (Bayes factors) to show that process heterogeneity across data partitions is a significant model component, although not as important as among-site rate variation. More complex evolutionary models are associated with more topological uncertainty and less conflict between morphology and molecules. Bayes factors sometimes favor simpler models over considerably more parameter-rich models, but the best model overall is also the most complex and Bayes factors do not support exclusion of apparently weak parameters from this model. Thus, Bayes factors appear to be useful for selecting among complex models, but it is still unclear whether their use strikes a reasonable balance between model complexity and error in parameter estimates.
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            The global economic cost of sea lice to the salmonid farming industry.

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              Crustacean appendage evolution associated with changes in Hox gene expression.

              Homeotic (Hox) genes specify the differential identity of segments along the body axis of insects. Changes in the segmental organization of arthropod bodies may therefore be driven by changes in the function of Hox genes, but so far this has been difficult to demonstrate. We show here that changes in the expression pattern of the Hox genes Ubx and AbdA in different crustaceans correlate well with the modification of their anterior thoracic limbs into feeding appendages (maxillipeds). Our observations provide direct evidence that major morphological changes in arthropod body plans are associated with changes in Hox gene regulation. They suggest that homeotic changes may play a role in the normal process of adaptive evolutionary change.
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                Author and article information

                Contributors
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central
                1756-3305
                2013
                28 November 2013
                : 6
                : 336
                Affiliations
                [1 ]Institute of Ocean and Earth Sciences, University of Malaya, Kuala Lumpur, Malaysia
                [2 ]Department of Fisheries, Laboratory of Fish Parasites and Diseases, Faculty of Marine Sciences and Fisheries, Hasanuddin University, Makassar, Indonesia
                [3 ]Meguro Parasitological Museum, 4-1-1, Shimomeguro, Meguro-ku, Tokyo 153-0064, Japan
                Article
                1756-3305-6-336
                10.1186/1756-3305-6-336
                4176263
                24286135
                e9c16d4d-a605-40e1-8445-4cf192ef3940
                Copyright © 2013 Freeman et al.; 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
                : 26 September 2013
                : 25 November 2013
                Categories
                Research

                Parasitology
                pseudocaligus,caligus,convergent evolution,caligidae,appendage reduction,lepeophtheirus,synapomorphy

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