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      Evidence for Paternal Leakage in Hybrid Periodical Cicadas (Hemiptera: Magicicada spp.)

      research-article
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      PLoS ONE
      Public Library of Science

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          Abstract

          Mitochondrial inheritance is generally assumed to be maternal. However, there is increasing evidence of exceptions to this rule, especially in hybrid crosses. In these cases, mitochondria are also inherited paternally, so “paternal leakage” of mitochondria occurs. It is important to understand these exceptions better, since they potentially complicate or invalidate studies that make use of mitochondrial markers. We surveyed F 1 offspring of experimental hybrid crosses of the 17-year periodical cicadas Magicicada septendecim, M. septendecula, and M. cassini for the presence of paternal mitochondrial markers at various times during development (1-day eggs; 3-, 6-, 9-week eggs; 16-month old 1 st and 2 nd instar nymphs). We found evidence of paternal leakage in both reciprocal hybrid crosses in all of these samples. The relative difficulty of detecting paternal mtDNA in the youngest eggs and ease of detecting leakage in older eggs and in nymphs suggests that paternal mitochondria proliferate as the eggs develop. Our data support recent theoretical predictions that paternal leakage may be more common than previously estimated.

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          Some genetic consequences of ice ages, and their role in divergence and speciation

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            The incomplete natural history of mitochondria.

            Mitochondrial DNA (mtDNA) has been used to study molecular ecology and phylogeography for 25 years. Much important information has been gained in this way, but it is time to reflect on the biology of the mitochondrion itself and consider opportunities for evolutionary studies of the organelle itself and its ecology, biochemistry and physiology. This review has four sections. First, we review aspects of the natural history of mitochondria and their DNA to show that it is a unique molecule with specific characteristics that differ from nuclear DNA. We do not attempt to cover the plethora of differences between mitochondrial and nuclear DNA; rather we spotlight differences that can cause significant bias when inferring demographic properties of populations and/or the evolutionary history of species. We focus on recombination, effective population size and mutation rate. Second, we explore some of the difficulties in interpreting phylogeographical data from mtDNA data alone and suggest a broader use of multiple nuclear markers. We argue that mtDNA is not a sufficient marker for phylogeographical studies if the focus of the investigation is the species and not the organelle. We focus on the potential bias caused by introgression. Third, we show that it is not safe to assume a priori that mtDNA evolves as a strictly neutral marker because both direct and indirect selection influence mitochondria. We outline some of the statistical tests of neutrality that can, and should, be applied to mtDNA sequence data prior to making any global statements concerning the history of the organism. We conclude with a critical examination of the neglected biology of mitochondria and point out several surprising gaps in the state of our knowledge about this important organelle. Here we limelight mitochondrial ecology, sexually antagonistic selection, life-history evolution including ageing and disease, and the evolution of mitochondrial inheritance.
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              The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models.

              C Birky (2001)
              The inheritance of mitochondrial and chloroplast genes differs from that of nuclear genes in showing vegetative segregation, uniparental inheritance, intracellular selection, and reduced recombination. Vegetative segregation and some cases of uniparental inheritance are due to stochastic replication and partitioning of organelle genomes. The rate and pattern of vegetative segregation depend partly on the numbers of genomes and of organelles per cell, but more importantly on the extent to which genomes are shared between organelles, their distribution in the cell, the variance in number of replications per molecule, and the variance in numerical and genotypic partitioning of organelles and genomes. Most of these parameters are unknown for most organisms, but a simple binomial probability model using the effective number of genomes is a useful substitute. Studies using new cytological, molecular, and genetic methods are shedding some light on the processes involved in segregation, and also on the mechanisms of intracellular selection and uniparental inheritance in mammals. But significant issues remain unresolved, notably about the extent of paternal transmission and mitochondrial fusion in mammals.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS ONE
                plos
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2007
                12 September 2007
                : 2
                : 9
                : e892
                Affiliations
                [1]Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut, United States of America
                Centre National de la Recherche Scientifique, France
                Author notes
                * To whom correspondence should be addressed. E-mail: john.cooley@ 123456uconn.edu

                Conceived and designed the experiments: CS JC KF. Performed the experiments: KF. Analyzed the data: JC KF. Contributed reagents/materials/analysis tools: CS KF. Wrote the paper: CS JC KF.

                [¤]

                Current address: Thayer School of Engineering, Dartmouth College, Hanover, New Hampshire, United States of America

                Article
                07-PONE-RA-01765R1
                10.1371/journal.pone.0000892
                1963320
                17849021
                f68e787b-b233-4aeb-8632-32d6938977fc
                Fontaine et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 16 July 2007
                : 23 August 2007
                Page count
                Pages: 8
                Categories
                Research Article
                Evolutionary Biology/Animal Genetics

                Uncategorized
                Uncategorized

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