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      Gone with the plate: the opening of the Western Mediterranean basin drove the diversification of ground-dweller spiders

      , 1 , 1

      BMC Evolutionary Biology

      BioMed Central

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          Abstract

          Background

          The major islands of the Western Mediterranean--Corsica, Sardinia, and the Balearic Islands--are continental terrenes that drifted towards their present day location following a retreat from their original position on the eastern Iberian Peninsula about 30 million years ago. Several studies have taken advantage of this well-dated geological scenario to calibrate molecular rates in species for which distributions seemed to match this tectonic event. Nevertheless, the use of external calibration points has revealed that most of the present-day fauna on these islands post-dated the opening of the western Mediterranean basin. In this study, we use sequence information of the cox1, nad1, 16S, L1, and 12S mitochondrial genes and the 18S, 28S, and h3 nuclear genes, along with relaxed clock models and a combination of biogeographic and fossil external calibration points, to test alternative historical scenarios of the evolutionary history of the ground-dweller spider genus Parachtes (Dysderidae), which is endemic to the region.

          Results

          We analyse 49 specimens representing populations of most Parachtes species and close relatives. Our results reveal that both the sequence of species formation in Parachtes and the estimated divergence times match the geochronological sequence of separation of the main islands, suggesting that the diversification of the group was driven by Tertiary plate tectonics. In addition, the confirmation that Parachtes diversification matches well-dated geological events provides a model framework to infer substitution rates of molecular markers. Divergence rates estimates ranged from 3.5% My -1 ( nad1) to 0.12% My -1 ( 28S), and the average divergence rate for the mitochondrial genes was 2.25% My -1, very close to the "standard" arthropod mitochondrial rate (2.3% My -1).

          Conclusions

          Our study provides the first unequivocal evidence of terrestrial endemic fauna of the major western Mediterranean islands, whose origin can be traced back to the Oligocene separation of these islands from the continent. Moreover, our study provides useful information on the divergence rate estimates of the most commonly used genes for phylogenetic inference in non-model arthropods.

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          Most cited references 70

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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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            Gene Trees in Species Trees

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              Time dependency of molecular rate estimates and systematic overestimation of recent divergence times.

              Studies of molecular evolutionary rates have yielded a wide range of rate estimates for various genes and taxa. Recent studies based on population-level and pedigree data have produced remarkably high estimates of mutation rate, which strongly contrast with substitution rates inferred in phylogenetic (species-level) studies. Using Bayesian analysis with a relaxed-clock model, we estimated rates for three groups of mitochondrial data: avian protein-coding genes, primate protein-coding genes, and primate d-loop sequences. In all three cases, we found a measurable transition between the high, short-term (< 1-2 Myr) mutation rate and the low, long-term substitution rate. The relationship between the age of the calibration and the rate of change can be described by a vertically translated exponential decay curve, which may be used for correcting molecular date estimates. The phylogenetic substitution rates in mitochondria are approximately 0.5% per million years for avian protein-coding sequences and 1.5% per million years for primate protein-coding and d-loop sequences. Further analyses showed that purifying selection offers the most convincing explanation for the observed relationship between the estimated rate and the depth of the calibration. We rule out the possibility that it is a spurious result arising from sequence errors, and find it unlikely that the apparent decline in rates over time is caused by mutational saturation. Using a rate curve estimated from the d-loop data, several dates for last common ancestors were calculated: modern humans and Neandertals (354 ka; 222-705 ka), Neandertals (108 ka; 70-156 ka), and modern humans (76 ka; 47-110 ka). If the rate curve for a particular taxonomic group can be accurately estimated, it can be a useful tool for correcting divergence date estimates by taking the rate decay into account. Our results show that it is invalid to extrapolate molecular rates of change across different evolutionary timescales, which has important consequences for studies of populations, domestication, conservation genetics, and human evolution.
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                Author and article information

                Journal
                BMC Evol Biol
                BMC Evolutionary Biology
                BioMed Central
                1471-2148
                2011
                31 October 2011
                : 11
                : 317
                Affiliations
                [1 ]Institut de Recerca de la Biodiversitat & Departament de Biologia Animal, Universitat de Barcelona, Av. Diagonal 643, 08020, Barcelona, Spain
                Article
                1471-2148-11-317
                10.1186/1471-2148-11-317
                3273451
                22039781
                Copyright ©2011 Bidegaray-Batista and Arnedo; 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.

                Categories
                Research Article

                Evolutionary Biology

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