Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA

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Abstract

There is only one exception to strict maternal inheritance of mitochondrial DNA (mtDNA) in the animal kingdom: a system named doubly uniparental inheritance (DUI), which is found in several bivalve species. Why and how such a radically different system of mitochondrial transmission evolved in bivalve remains obscure. Obtaining a more complete taxonomic distribution of DUI in the Bivalvia may help to better understand its origin and function. In this study we provide evidence for the presence of sex-linked heteroplasmy (thus the possible presence of DUI) in two bivalve species, i.e., the nuculanoid Yoldia hyperborea(Gould, 1841)and the veneroid Scrobicularia plana(Da Costa ,1778), increasing the number of families in which DUI has been found by two. An update on the taxonomic distribution of DUI in the Bivalvia is also presented.

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Dating of the human-ape splitting by a molecular clock of mitochondrial DNA.

H Kishino, T Yano, M. Hasegawa (1984)

A new statistical method for estimating divergence dates of species from DNA sequence data by a molecular clock approach is developed. This method takes into account effectively the information contained in a set of DNA sequence data. The molecular clock of mitochondrial DNA (mtDNA) was calibrated by setting the date of divergence between primates and ungulates at the Cretaceous-Tertiary boundary (65 million years ago), when the extinction of dinosaurs occurred. A generalized least-squares method was applied in fitting a model to mtDNA sequence data, and the clock gave dates of 92.3 +/- 11.7, 13.3 +/- 1.5, 10.9 +/- 1.2, 3.7 +/- 0.6, and 2.7 +/- 0.6 million years ago (where the second of each pair of numbers is the standard deviation) for the separation of mouse, gibbon, orangutan, gorilla, and chimpanzee, respectively, from the line leading to humans. Although there is some uncertainty in the clock, this dating may pose a problem for the widely believed hypothesis that the pipedal creature Australopithecus afarensis, which lived some 3.7 million years ago at Laetoli in Tanzania and at Hadar in Ethiopia, was ancestral to man and evolved after the human-ape splitting. Another likelier possibility is that mtDNA was transferred through hybridization between a proto-human and a proto-chimpanzee after the former had developed bipedalism.

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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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Resolving the evolutionary relationships of molluscs with phylogenomic tools.

Casey W. Dunn, Edward N Wilson, Gonzalo Giribet … (2011)

Molluscs (snails, octopuses, clams and their relatives) have a great disparity of body plans and, among the animals, only arthropods surpass them in species number. This diversity has made Mollusca one of the best-studied groups of animals, yet their evolutionary relationships remain poorly resolved. Open questions have important implications for the origin of Mollusca and for morphological evolution within the group. These questions include whether the shell-less, vermiform aplacophoran molluscs diverged before the origin of the shelled molluscs (Conchifera) or lost their shells secondarily. Monoplacophorans were not included in molecular studies until recently, when it was proposed that they constitute a clade named Serialia together with Polyplacophora (chitons), reflecting the serial repetition of body organs in both groups. Attempts to understand the early evolution of molluscs become even more complex when considering the large diversity of Cambrian fossils. These can have multiple dorsal shell plates and sclerites or can be shell-less but with a typical molluscan radula and serially repeated gills. To better resolve the relationships among molluscs, we generated transcriptome data for 15 species that, in combination with existing data, represent for the first time all major molluscan groups. We analysed multiple data sets containing up to 216,402 sites and 1,185 gene regions using multiple models and methods. Our results support the clade Aculifera, containing the three molluscan groups with spicules but without true shells, and they support the monophyly of Conchifera. Monoplacophora is not the sister group to other Conchifera but to Cephalopoda. Strong support is found for a clade that comprises Scaphopoda (tusk shells), Gastropoda and Bivalvia, with most analyses placing Scaphopoda and Gastropoda as sister groups. This well-resolved tree will constitute a framework for further studies of mollusc evolution, development and anatomy.

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Author and article information

Contributors

Sophie Breton

Journal

Journal ID (nlm-ta): PeerJ

Journal ID (iso-abbrev): PeerJ

Journal ID (publisher-id): peerj

Journal ID (pmc): peerj

Title: PeerJ

Publisher: PeerJ Inc. (San Francisco, USA )

ISSN (Electronic): 2167-8359

Publication date (Electronic): 13 December 2016

Publication date Collection: 2016

Volume: 4

Electronic Location Identifier: e2760

Affiliations

[1 ]Department of Biological Sciences, Université de Montréal , Montréal, Québec, Canada

[2 ]Department of Biological Sciences, Université de Strasbourg , Strasbourg, France

[3 ]Department of Biology, Acadia University , Wolfville, Nova Scotia, Canada

[4 ]Department of Biological Geological and Environmental Sciences, University of Bologna , Bologna, Italy

Article

Publisher ID: 2760

DOI: 10.7717/peerj.2760

PMC ID: 5157197

PubMed ID: 27994972

SO-VID: 8d480b82-4992-452b-904e-0d89f341a7b9

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This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

History

Date received : 4 September 2016

Date accepted : 5 November 2016

Funding

Funded by: Natural Sciences and Engineering Research Council of Canada

Award ID: RGPIN/435656-2013

Award ID: RGPIN/217175-2013

Funded by: ‘Canziani Bequest’ and ‘Fondazione del Monte’

Funded by: Groupe de Recherche Interuniversitaire en Limnologie et en environnement aquatique (GRIL)

Funded by: Faculté des Études Supérieures et Postdoctorales (FESP) of the University of Montreal

This work was supported by funding from the Natural Sciences and Engineering Research Council of Canada (grant no., RGPIN/435656-2013 to S.B. and grant no., RGPIN/217175-2013 to D.T.S.), and by ‘Canziani Bequest’ and ‘Fondazione del Monte’ funding (M.P.). A.G. was financially supported by the Groupe de Recherche Interuniversitaire en Limnologie et en environnement aquatique (GRIL) and by the Faculté des Études Supérieures et Postdoctorales (FESP) of the University of Montreal. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Pursuing the quest for better understanding the taxonomic distribution of the system of doubly uniparental inheritance of mtDNA

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Abstract

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Taxonomic intelligence

Most cited references 85

Dating of the human-ape splitting by a molecular clock of mitochondrial DNA.

The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models.

Resolving the evolutionary relationships of molluscs with phylogenomic tools.

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