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      Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes

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          Abstract

          Background

          One of the main explanations for the stunning diversity of teleost fishes (~29,000 species, nearly half of all vertebrates) is that a fish-specific whole-genome duplication event (FSGD) in the ancestor to teleosts triggered their subsequent radiation. However, one critical assumption of this hypothesis, that diversification rates in teleosts increased soon after the acquisition of a duplicated genome, has never been tested.

          Results

          Here we show that one of three major diversification rate shifts within ray-finned fishes occurred at the base of the teleost radiation, as predicted by the FSGD hypothesis. We also find evidence for two rate increases that are much younger than the inferred age of the FSGD: one in the common ancestor of most ostariophysan fishes, and a second one in the common ancestor of percomorphs. The biodiversity contained within these two clades accounts for more than 88% of living fish species.

          Conclusion

          Teleosts diversified explosively in their early history and this burst of diversification may have been caused by genome duplication. However, the FSGD itself may be responsible for a little over 10% of living teleost biodiversity. ~88% of species diversity is derived from two relatively recent radiations of freshwater and marine fishes where genome duplication is not suspected. Genome duplications are a common event on the tree of life and have been implicated in the diversification of major clades like flowering plants, vertebrates, and gnathostomes. However our results suggest that the causes of diversification in large clades are likely to be complex and not easily ascribed to a single event, even a dramatic one such as a whole genome duplication.

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          Most cited references35

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          Chronology of fluctuating sea levels since the triassic.

          Advances in sequence stratigraphy and the development of depositional models have helped explain the origin of genetically related sedimentary packages during sea level cycles. These concepts have provided the basis for the recognition of sea level events in subsurface data and in outcrops of marine sediments around the world. Knowledge of these events has led to a new generation of Mesozoic and Cenozoic global cycle charts that chronicle the history of sea level fluctuations during the past 250 million years in greater detail than was possible from seismic-stratigraphic data alone. An effort has been made to develop a realistic and accurate time scale and widely applicable chronostratigraphy and to integrate depositional sequences documented in public domain outcrop sections from various basins with this chronostratigraphic framework. A description of this approach and an account of the results, illustrated by sea level cycle charts of the Cenozoic, Cretaceous, Jurassic, and Triassic intervals, are presented.
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            The probability of duplicate gene preservation by subfunctionalization.

            It has often been argued that gene-duplication events are most commonly followed by a mutational event that silences one member of the pair, while on rare occasions both members of the pair are preserved as one acquires a mutation with a beneficial function and the other retains the original function. However, empirical evidence from genome duplication events suggests that gene duplicates are preserved in genomes far more commonly and for periods far in excess of the expectations under this model, and whereas some gene duplicates clearly evolve new functions, there is little evidence that this is the most common mechanism of duplicate-gene preservation. An alternative hypothesis is that gene duplicates are frequently preserved by subfunctionalization, whereby both members of a pair experience degenerative mutations that reduce their joint levels and patterns of activity to that of the single ancestral gene. We consider the ways in which the probability of duplicate-gene preservation by such complementary mutations is modified by aspects of gene structure, degree of linkage, mutation rates and effects, and population size. Even if most mutations cause complete loss-of-subfunction, the probability of duplicate-gene preservation can be appreciable if the long-term effective population size is on the order of 10(5) or smaller, especially if there are more than two independently mutable subfunctions per locus. Even a moderate incidence of partial loss-of-function mutations greatly elevates the probability of preservation. The model proposed herein leads to quantitative predictions that are consistent with observations on the frequency of long-term duplicate gene preservation and with observations that indicate that a common fate of the members of duplicate-gene pairs is the partitioning of tissue-specific patterns of expression of the ancestral gene.
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              Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates.

              The uneven distribution of species richness is a fundamental and unexplained pattern of vertebrate biodiversity. Although species richness in groups like mammals, birds, or teleost fishes is often attributed to accelerated cladogenesis, we lack a quantitative conceptual framework for identifying and comparing the exceptional changes of tempo in vertebrate evolutionary history. We develop MEDUSA, a stepwise approach based upon the Akaike information criterion for detecting multiple shifts in birth and death rates on an incompletely resolved phylogeny. We apply MEDUSA incompletely to a diversity tree summarizing both evolutionary relationships and species richness of 44 major clades of jawed vertebrates. We identify 9 major changes in the tempo of gnathostome diversification; the most significant of these lies at the base of a clade that includes most of the coral-reef associated fishes as well as cichlids and perches. Rate increases also underlie several well recognized tetrapod radiations, including most modern birds, lizards and snakes, ostariophysan fishes, and most eutherian mammals. In addition, we find that large sections of the vertebrate tree exhibit nearly equal rates of origination and extinction, providing some of the first evidence from molecular data for the importance of faunal turnover in shaping biodiversity. Together, these results reveal living vertebrate biodiversity to be the product of volatile turnover punctuated by 6 accelerations responsible for >85% of all species as well as 3 slowdowns that have produced "living fossils." In addition, by revealing the timing of the exceptional pulses of vertebrate diversification as well as the clades that experience them, our diversity tree provides a framework for evaluating particular causal hypotheses of vertebrate radiations.
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                Author and article information

                Journal
                BMC Evol Biol
                BMC Evolutionary Biology
                BioMed Central
                1471-2148
                2009
                8 August 2009
                : 9
                : 194
                Affiliations
                [1 ]Department of Ecology and Evolutionary Biology, University of California at Los Angeles, 651 Charles Young Dr. South, Los Angeles, CA 90095, USA
                [2 ]Department of Biology, University of Idaho, Moscow, ID 83844, USA
                [3 ]Dipartimento di Scienze della Terra, Universitá di Pisa, Via Santa Maria 53, 56126 Pisa, Italy
                [4 ]Museo di Storia Naturale e del Territorio, Via Roma 79, 56011, Calci, Italy
                Article
                1471-2148-9-194
                10.1186/1471-2148-9-194
                2743667
                19664233
                4139e33d-7f12-402b-9499-1fcd3bc6722c
                Copyright © 2009 Santini 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
                : 9 December 2008
                : 8 August 2009
                Categories
                Research Article

                Evolutionary Biology
                Evolutionary Biology

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