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      Phylogenetic evidence for recent diversification of obligate coral-dwelling gobies compared with their host corals

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          Graphical abstract

          Highlights

          • The coral reef-dwelling genus Gobiodon diversified within the last 10 My.

          • Acroporid hosts of Gobiodon fishes have radiated since the Eocene (49 Mya).

          • Despite a mutualistic association Gobiodon fishes did not co-speciate with corals.

          • Testing dates of diversification is fundamental before assuming co-speciation.

          • Phylogenetics of Gobiodon differ in part with previous morphological analyses.

          Abstract

          The rich diversity of coral reef organisms is supported, at least in part, by the diversity of coral reef habitat. Some of the most habitat specialised fishes on coral reefs are obligate coral-dwelling gobies of the genus Gobiodon that inhabit a range of coral species, mostly of the genus Acropora. However, the role of this specialised pattern of habitat use in the evolution of coral-dwelling gobies is not well understood. Diversification of coral-dwelling gobies may be driven by the diversification of their host corals (cospeciation), or alternatively, diversification of these fishes may have occurred independently of the diversification of host corals. The cospeciation hypothesis assumes similar timing in evolution of the gobies and their host corals. We used four genes for each group and the available fossil records to reconstruct and date phylogenies for 20 species of Gobiodon from the Indo-Pacific and the Red Sea, and for 28 species of the coral genus Acropora. Our results indicate that Gobiodon diversified mostly in the last ∼5 My, whereas Acropora corals have consistently diversified since the Eocene, making the hypothesis of cospeciation untenable. The fully resolved molecular phylogeny of the genus Gobiodon is in part at odds with previous analyses incorporating morphological data and indicates that some morphological traits form paraphyletic clades within Gobiodon. Our phylogeny supports a hypothesis in which Gobiodon diversified in the Indo-Pacific Ocean and then radiated recently, with multiple new variants found in the Red Sea.

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          Most cited references 71

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          MRBAYES: Bayesian inference of phylogenetic trees.

          The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
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            Hybridization and speciation.

            Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky-Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization. © 2013 The Authors. Journal of Evolutionary Biology © 2013 European Society For Evolutionary Biology.
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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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                Author and article information

                Contributors
                Journal
                Mol Phylogenet Evol
                Mol. Phylogenet. Evol
                Molecular Phylogenetics and Evolution
                Academic Press
                1055-7903
                1095-9513
                1 October 2013
                October 2013
                : 69
                : 1
                : 123-132
                Affiliations
                [a ]School of Marine and Tropical Biology, James Cook University, Townsville, QLD 4811, Australia
                [b ]School of Medicine, University of Sydney, Sydney, NSW 2006, Australia
                [c ]ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811, Australia
                [d ]Department of Integrative Zoology, Faculty of Life Sciences, University of Vienna, Vienna, Austria
                [e ]Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, QLD 4811, Australia
                Author notes
                [* ]Corresponding author. Current address: Gould Building (Bldg. 116), Daley Road, The Australian National University, Canberra, ACT 0200, Australia. Fax: +61 2 6125 5573. david.duchene@ 123456anu.edu.au
                Article
                S1055-7903(13)00191-7
                10.1016/j.ympev.2013.04.033
                4047829
                23680856
                © 2013 The Authors

                This is an open access article under the CC BY-NC-SA license (http://creativecommons.org/licenses/by-nc-sa/3.0/).

                Categories
                Article

                Evolutionary Biology

                cospeciation, mutualism, coral reef, gobiodon, molecular dating, acropora

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