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Mitochondrial Genomes of the Baltic Clam Macoma Balthica (Bivalvia

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Mitochondrial Genomes of the Baltic Clam Macoma Balthica (Bivalvia Saunier et al. BMC Evolutionary Biology ( DOI 10.1186/s12862-014-0259-z RESEARCH ARTICLE Open Access Mitochondrial genomes of the Baltic clam Macoma balthica (Bivalvia: Tellinidae): setting the stage for studying mito-nuclear incompatibilities Alice Saunier1*, Pascale Garcia1, Vanessa Becquet1, Nathalie Marsaud2, Frédéric Escudié2 and Eric Pante1* Abstract Background: Allopatric divergence across lineages can lead to post-zygotic reproductive isolation upon secondary contact and disrupt coevolution between mitochondrial and nuclear genomes, promoting emergence of genetic incompatibilities. A previous FST scan on the transcriptome of the Baltic clam Macoma balthica highlighted several genes potentially involved in mito-nuclear incompatibilities (MNIs). As proteins involved in the mitochondrial oxidative phosphorylation(OXPHO)chainarepronetoMNIsandcancontributetothemaintenanceofgeneticbarriers,the mitochondrial genomes of six Ma. balthica individuals spanning two secondary contact zones were sequenced using the Illumina MiSeq plateform. Results: The mitogenome has an approximate length of 16,806 bp and encodes 13 protein-coding genes, 2 rRNAs and 22 tRNAs, all located on the same strand. atp8, a gene long reported as rare in bivalves, was detected. It encodes 42 amino acids and is putatively expressed and functional. A large unassigned region was identified between rrnS and tRNAMet and could likely correspond to the Control Region. Replacement and synonymous mutations were mapped on the inferred secondary structure of all protein-coding genes of the OXPHO chain. The atp6 and atp8 genes were characterized by background levels of replacement mutations, relative to synonymous mutations. However, most nad genes (notably nad2 and nad5) were characterized by an elevated proportion of replacement mutations. Conclusions: Six nearly complete mitochondrial genomes were successfully assembled and annotated, providing the necessary roadmap to study MNIs at OXPHO loci. Few replacement mutations were mapped on mitochondrial-encoded ATP synthase subunits, which is in contrast with previous data on nuclear-encoded subunits. Conversely, the high population divergence and the prevalence of non-synonymous mutations at nad genes are congruent with previous observations from the nuclear transcriptome. This further suggest that MNIs between subunits of Complex I of the OXPHO chain, coding for NADH dehydrogenase, may play a role in maintaining barriers to gene flow in Ma. balthica. Keywords: NADH dehydrogenase, ATP synthase, Next-generation sequencing, OXPHO chain, Positive selection, Inter-specific hybridization, Hybrid zone * Correspondence: [email protected]; [email protected] 1Littoral, Environnement et Sociétés, UMR 7266 CNRS, Université de La Rochelle, 2 rue Olympe de Gouges, La Rochelle 17000, France Full list of author information is available at the end of the article © 2014 Saunier et al.; licensee BioMed Central. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Saunier et al. BMC Evolutionary Biology ( Page 2 of 13 Background complexes are composed of subunits encoded by both The mitochondrial electron transport chain, a central nuclear and mitochondrial genes [2] and require tight component of cellular energy production, relies on the mito-nuclear coevolution to be fully operational. They are coevolution of mitochondrial- and nuclear-encoded genes therefore prime candidates for the establishment of MNIs to function [1,2]. Mito-nuclear coevolution is however following secondary contact between previously allopatric easily disrupted because genomes have different mutation populations [6,17], which may constitute endogenous bar- rates, modes of inheritance, number and speed of recom- riers to gene flow. bination events, effective population size and selection Sequences from only two mitochondrial genes have pressures [3-5]. Such disruption can cause the emergence been published to date for this species (cox3 [22]; cox1 and maintenance of mito-nuclear incompatibilities (MNIs, [21,23]). To work toward the diagnosis of MNIs in Ma. among other types of genomic incompatibilities [6-9]) that balthica and further test the hypothesis of mito-nuclear are described by the Dobzhansky-Muller model [10,11]. coevolution breakdown among Ma. balthica lineages, Dobzhansky-Muller incompatibilities have been impli- additional mitochondrial data are therefore required for cated in intrinsic post-zygotic barriers [8] and involved in comparison with the nuclear transcriptomic data at hand. mito-nuclear gene interactions in the fruit fly Drosophila Although several mitogenomes have been sequenced for [5], the parasitoid wasp Nasonia [12-14], the Atlantic eel marine bivalves (e.g. [25,26]) only one is currently available Anguilla [15,16] and the marine copepod Trigriopus cali- for the Tellinidae (Moerella iridescens [26]). However, fornicus [4,17,18]. Studying reproductive isolation is espe- mitochondrial sequences of Mo. iridescens are highly cially relevant in the marine environment, where many divergent from those of Ma. balthica (raw p-distance at marine organisms have a high fecundity, large population cox1 of 17%). We have therefore set to sequence the mito- sizes and a high dispersive potential [19], and where genomes of six Ma. balthica individuals spanning two physical barriers to dispersal are not readily apparent. secondary contact zones (i.e. across the Kattegat strait and Endogenous barriers to gene flow may therefore be an the Brittany peninsula) to test whether mitochondrial important factor structuring marine populations in this genes interacting with previously-detected nuclear outlier environment. In addition, marine taxa can be sensitive loci show stronger divergence and selection pressures, to glaciation cycles that can promote the establishment compared to other mitochondrial genes. Our intents were of secondary contact zones and therefore lead to admix- (i) to detect and map protein-coding genes (PCGs) in- ture of genetically divergent backgrounds [20]. volved in the OXPHO chain, (ii) to estimate the degree of In this context, the Baltic clam Macoma balthica divergence and selection pressures across lineages for all (Mollusca: Bivalvia: Tellinidae) is a noteworthy model PCGs, and (iii) to map mutations onto predicted second- for studying the role of MNIs in structuring marine ary structure of mitochondrial membrane-embedded pro- populations. This infaunal tellinid bivalve occurs on sandy- tein to help detect potential incompatibilities among mud flats from the upper intertidal to the subtidal, in mitochondrial and nuclear OXPHO subunits. In particu- parts of the northern hemisphere. Its natural European lar, we characterize a putative atp8 gene and discuss its range extends from eastern Russia (Pechora Sea) to functionality, as (i) it is absent in about half of the pub- southern France (Gironde Estuary). Ma. balthica is lished bivalve mitogenomes, and (ii) its role is potentially characterized by a complex colonization history in Europe. relevant to the study of MNIs in Ma. balthica. With the opening of the Bering Strait, several trans-arctic invasion events of Pacific populations into the Atlantic Methods have occurred, leading to secondary contact of divergent Sample collection and DNA extraction lineages in the Bay of Biscay [21] and in the Baltic and Previous work on Ma. balthica suggested the presence White seas [22], allowing gene flow between previously- of at least three divergent mitochondrial clades in Europe isolated populations. The long periods of reproductive [21-23], which were targeted in our sampling: a Baltic isolation between these populations (~0.1-1.8 My between lineage, and two Atlantic lineages that are separated by Bay of Biscay populations [23]; ~ 2–3.5 My between Ma. the French Finistère peninsula. Ma. balthica specimens balthica balthica and Ma. balthica rubra subspecies [22]) were collected from 2003 to 2006 (A10, M12, W4, W20 represent strong potential for the accumulation of genetic and F17) and 2013 (A6) along European coasts, ranging incompatibilities. from Aytré, France to Tvärminne, Finland (Table 1). A recent FST scan based on transcriptome data Total genomic DNA was extracted from foot muscle highlighted outlier loci coding for nuclear subunits of tissue using the Dneasy™ Tissue Kit (Qiagen, Germany) the FOF1-ATP synthase complex (subunits alpha, gamma following the manufacturer's protocol and stored at −20°C and O) and a putative isoform of the NADH deshydrogen- until further analyses. ase [24], which are involved in the oxidative phosphoryl- Initially eight mitogenomes were sequenced, corre- ation (OXPHO) mitochondrial chain [1,2]. These protein sponding to two individuals per mitochondrial lineage, Saunier et al. BMC Evolutionary Biology ( Page 3 of 13 Table 1 Sampling sites and mitochondrial cox1 haplotypes of the sequenced specimens of Ma. balthica. cox1 haplotypes are described in Becquet et al. [21] and are noted H1 to H5. H1 and H2 are common of the Bay of Biscay, H3 of the English Channel, H4 and H5 of North and Baltic seas, respectively Sampling site Country Code Latitude Longitude
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