Mitogenome Variation Research Articles

Forensically relevant phylogeographic evaluation of mitogenome variation in the Basque Country

The Basque Country has been the focus of population (genetic) and evolutionary studies for decades, as it represents an interesting evolutionary feature: it is the only European country where a non-Indo-European language is still spoken today and, for which there are no known living or extinct relatives. Early studies that were based on anatomical and serological methods, along with subsequent molecular genetic investigations, contain controversial interpretations of their data. Additionally, the analysis of mitochondrial DNA, which is maternally inherited and thus suitable for the examination of the maternal phylogeny of the population, was the focus of some studies. Early mtDNA studies were however restricted to the information provided by the control region or its hypervariable segments only. These are known to harbour little phylogenetic information, particularly for haplogroup H that is dominant in Westeurasian populations including the Basques. Later studies analysed complete mitogenome sequences. Their information content is however limited, either because the number of samples was low, or because these studies only considered particular haplogroups. In this study we present the full mitogenome sequences of 178 autochthonous Basque individuals that were carefully selected based on their familial descent and discuss the observed phylogenetic signals in the light of earlier published findings. We confirm the presence of Basque-specific mtDNA lineages and extend the knowledge of these lineages by providing data on their distribution in comparison to other Basque and non-Basque populations. This dataset improves our understanding of the Basque mtDNA phylogeny and serves as a high-quality dataset that is provided via EMPOP for forensic genetic purposes.

Mobile genetic elements explain size variation in the mitochondrial genomes of four closely-related Armillaria species

BackgroundSpecies in the genus Armillaria (fungi, basidiomycota) are well-known as saprophytes and pathogens on plants. Many of them cause white-rot root disease in diverse woody plants worldwide. Mitochondrial genomes (mitogenomes) are widely used in evolutionary and population studies, but despite the importance and wide distribution of Armillaria, the complete mitogenomes have not previously been reported for this genus. Meanwhile, the well-supported phylogeny of Armillaria species provides an excellent framework in which to study variation in mitogenomes and how they have evolved over time.ResultsHere we completely sequenced, assembled, and annotated the circular mitogenomes of four species: A. borealis, A. gallica, A. sinapina, and A. solidipes (116,443, 98,896, 103,563, and 122,167 bp, respectively). The variation in mitogenome size can be explained by variable numbers of mobile genetic elements, introns, and plasmid-related sequences. Most Armillaria introns contained open reading frames (ORFs) that are related to homing endonucleases of the LAGLIDADG and GIY-YIG families. Insertions of mobile elements were also evident as fragments of plasmid-related sequences in Armillaria mitogenomes. We also found several truncated gene duplications in all four mitogenomes.ConclusionsOur study showed that fungal mitogenomes have a high degree of variation in size, gene content, and genomic organization even among closely related species of Armillara. We suggest that mobile genetic elements invading introns and intergenic sequences in the Armillaria mitogenomes have played a significant role in shaping their genome structure. The mitogenome changes we describe here are consistent with widely accepted phylogenetic relationships among the four species.

Global phylogeography reveals the origin and the evolutionary history of the gypsy moth (Lepidoptera, Erebidae)

We examined the global phylogeography of gypsy moth (Lymantria dispar L.) using molecular data based on mitochondrial and nuclear genes. Populations from all biogeographic regions of the native and introduced range of L. dispar, were sampled to fully document intraspecific and subspecies variation, identify potential cryptic species, and to clarify the relationships among major phylogeographic lineages. We recovered three major mtDNA lineages of L. dispar: Transcaucasia; East Asia + Japan; and Europe + Central Asia. The circumscription of these lineages is only partially consistent with the current taxonomic concept (i.e., L. dispar dispar; L. dispar asiatica; L. dispar japonica), with the following important discrepancies: (1) north-central Asian populations, including topotypical populations of L. dispar asiatica, may be more closely related to European rather than Asian segregates, which would require the synonymization of the taxon asiatica and establishment of a new name; (2) the Japanese populations (L. d. japonica) are not distinct from east Asian populations; (3) the presence of a distinct, unnamed mitogenomic lineage endemic to the Trancaucasus region. We demonstrated that the population from Transcaucasia contains the highest mitochondrial haplotype diversity among L. dispar, potentially indicative of an ancestral area for the entire dispar-group. Our study corroborates the endemic Hokkaido, Japan taxon Lymantria umbrosa (Butler) as the sister group to all other L. dispar populations, but the applicability of the names umbrosa versus hokkaidoensis Goldschmidt needs to be re-evaluated. The ancestral area analysis suggest that Japan was likely colonized via Sakhalin ∼1 Mya, in contrast to previous studies which have suggested colonization of the Japanese archipelago via the Korean Peninsula. Lastly, mitogenomic variation within L. dispar is incongruent with phylogenies based on nuclear DNA, as nDNA gene phylogenies did not recover the three major mtDNA lineages, and also failed to recover L. dispar and L. umbrosa as reciprocally monophyletic.

Analysis of the impact of cytoplasmic and mitochondrial inheritance on litter size and carcass in rabbits

<p>The effects of mitogenome variation on economically important traits have been reported in a number of domestic animal species. In this study, the first of its kind on rabbits, we have performed the estimation of the contribution of cytoplasmic and D-loop mitochondrial DNA (mtDNA) sequence effects on the litter size and carcass traits in three Pannon rabbit breeds (Pannon Ka, Pannon Large and Pannon White). The observed effects of both estimates, coming from cytoplasmic or D-loop mtDNA variation, were negligible. The most likely explanation for the results obtained is the lack of mitogenome polymorphism in all three populations, as suggested from the analysis performed on the D-loop mtDNA sequence, here assigned to the two most frequent rabbit haplotypes. The extent of potential benefits of the introduction, or alteration, of mitogenome variation in rabbit breeding remains an open question for future research.</p>

Convergent herbivory on conifers by Choristoneura moths after boreal forest formation

Mitogenomes are useful markers for phylogenetic studies across a range of taxonomic levels. Here, we focus on mitogenome variation across the tortricid moth genus Choristoneura and particularly the spruce budworm (Choristoneura fumiferana) species complex, a notorious pest group of North American conifer forests. Phylogenetic relationships of Tortricidae, representing two subfamilies, four tribes and nine genera, were analyzed using 21 mitogenomes. These included six newly-sequenced mitogenomes for species in the spruce budworm complex plus three additional Choristoneura species and 12 previously published mitogenomes from other tortricids and one from the Cossidae. We evaluated the phylogenetic informativeness of the mitogenomes and reconstructed a time-calibrated tree with fossil and secondary calibrations. We found that tortricid mitogenomes had conserved protein and ribosomal regions, and analysis of all protein-coding plus ribosomal genes together provided an efficient marker at any taxonomic rank. The time-calibrated phylogeny showed evolutionary convergence of conifer feeding within Choristoneura, with two independent lineages, the Nearctic spruce budworm complex and the Palearctic species Choristoneura murinana, both shifting onto conifers about 11 million years ago from angiosperms. These two host-plant shifts both occurred after the formation of boreal forest in the late Miocene. Haplotype diversification within the spruce budworm complex occurred in the last 4 million years, and is probably linked to the initial cooling cycles of the Northern Hemisphere in the Pliocene.

Genetic Drift and Indel Mutation in the Evolution of Yeast Mitochondrial Genome Size.

Mitochondrial genomes (mitogenomes) are remarkably diverse in genome size and organization, but the origins of dynamic mitogenome architectures are still poorly understood. For instance, the mutational burden hypothesis postulates that the drastic difference between large plant mitogenomes and streamlined animal mitogenomes can be driven by their different mutation rates. However, inconsistent trends between mitogenome sizes and mutation rates have been documented in several lineages. These conflicting results highlight the need of systematic and sophisticated investigations on the evolution and diversity of mitogenome architecture. This study took advantage of the strikingly variable mitogenome size among different yeast species and also among intraspecific strains, examined sequence dynamics of introns, GC-clusters, tandem repeats, mononucleotide repeats (homopolymers) and evaluated their contributions to genome size variation. The contributions of these sequence features to mitogenomic variation are dependent on the timescale, over which extant genomes evolved from their last common ancestor, perhaps due to a combination of different turnover rates of mobile sequences, variable insertion spaces, and functional constraints. We observed a positive correlation between mitogenome size and the level of genetic drift, suggesting that mitogenome expansion in yeast is likely driven by multiple types of sequence insertions in a primarily nonadaptive manner. Although these cannot be explained directly by the mutational burden hypothesis, our results support an important role of genetic drift in the evolution of yeast mitogenomes.

Mitochondrial genomes of the green macroalga Ulva pertusa (Ulvophyceae, Chlorophyta): novel insights into the evolution of mitogenomes in the Ulvophyceae.

To further understand the trends in the evolution of mitochondrial genomes (mitogenomes or mtDNAs) in the Ulvophyceae, the mitogenomes of two separate thalli of Ulva pertusa were sequenced. Two U.pertusa mitogenomes (Up1 and Up2) were 69,333bp and 64,602bp in length. These mitogenomes shared two ribosomal RNAs (rRNAs), 28 transfer RNAs (tRNAs), 29 protein-coding genes, and 12 open reading frames. The 4.7kb difference in size was attributed to variation in intron content and tandem repeat regions. A total of six introns were present in the smaller U.pertusa mtDNA (Up2), while the larger mtDNA (Up1) had eight. The larger mtDNA had two additional group II introns in two genes (cox1 and cox2) and tandem duplication mutations in noncoding regions. Our results showed the first case of intraspecific variation in chlorophytan mitogenomes and provided further genomic data for the undersampled Ulvophyceae.

Extreme Mitogenomic Variation in Natural Populations of Chaetognaths.

The extent of within-species genetic variation across the diversity of animal life is an underexplored problem in ecology and evolution. Although neutral genetic variation should scale positively with population size, mitochondrial diversity levels are believed to show little variation across animal species. Here, we report an unprecedented case of extreme mitochondrial diversity within natural populations of two morphospecies of chaetognaths (arrow worms). We determine that this diversity is composed of deep sympatric mitochondrial lineages, which are in some cases as divergent as human and platypus. Additionally, based on 54 complete mitogenomes, we observed mitochondrial gene order differences between several of these lineages. We examined nuclear divergence patterns (18S, 28S, and an intron) to determine the possible origin of these lineages, but did not find congruent patterns between mitochondrial and nuclear markers. We also show that extreme mitochondrial divergence in chaetognaths is not driven by positive selection. Hence, we propose that the extreme levels of mitochondrial variation could be the result of either a complex scenario of reproductive isolation, or a combination of large population size and accelerated mitochondrial mutation rate. These findings emphasize the importance of characterizing genome-wide levels of nuclear variation in these species and promote chaetognaths as a remarkable model to study mitochondrial evolution.

The Worldwide Spread of the Tiger Mosquito as Revealed by Mitogenome Haplogroup Diversity.

In the last 40 years, the Asian tiger mosquito Aedes albopictus, indigenous to East Asia, has colonized every continent except Antarctica. Its spread is a major public health concern, given that this species is a competent vector for numerous arboviruses, including those causing dengue, chikungunya, West Nile, and the recently emerged Zika fever. To acquire more information on the ancestral source(s) of adventive populations and the overall diffusion process from its native range, we analyzed the mitogenome variation of 27 individuals from representative populations of Asia, the Americas, and Europe. Phylogenetic analyses revealed five haplogroups in Asia, but population surveys appear to indicate that only three of these (A1a1, A1a2, and A1b) were involved in the recent worldwide spread. We also found out that a derived lineage (A1a1a1) within A1a1, which is now common in Italy, most likely arose in North America from an ancestral Japanese source. These different genetic sources now coexist in many of the recently colonized areas, thus probably creating novel genomic combinations which might be one of the causes of the apparently growing ability of A. albopictus to expand its geographical range.

Mitochondrial Genome Variation after Hybridization and Differences in the First and Second Generation Hybrids of Bream Fishes.

Hybridization plays an important role in fish breeding. Bream fishes contribute a lot to aquaculture in China due to their economically valuable characteristics and the present study included five bream species, Megalobrama amblycephala, Megalobrama skolkovii, Megalobrama pellegrini, Megalobrama terminalis and Parabramis pekinensis. As maternal inheritance of mitochondrial genome (mitogenome) involves species specific regulation, we aimed to investigate in which way the inheritance of mitogenome is affected by hybridization in these fish species. With complete mitogenomes of 7 hybrid groups of bream species being firstly reported in the present study, a comparative analysis of 17 mitogenomes was conducted, including representatives of these 5 bream species, 6 first generation hybrids and 6 second generation hybrids. The results showed that these 17 mitogenomes shared the same gene arrangement, and had similar gene size and base composition. According to the phylogenetic analyses, all mitogenomes of the hybrids were consistent with a maternal inheritance. However, a certain number of variable sites were detected in all F1 hybrid groups compared to their female parents, especially in the group of M. terminalis (♀) × M. amblycephala (♂) (MT×MA), with a total of 86 variable sites between MT×MA and its female parent. Among the mitogenomes genes, the protein-coding gene nd5 displayed the highest variability. The number of variation sites was found to be related to phylogenetic relationship of the parents: the closer they are, the lower amount of variation sites their hybrids have. The second generation hybrids showed less mitogenome variation than that of first generation hybrids. The non-synonymous and synonymous substitution rates (dN/dS) were calculated between all the hybrids with their own female parents and the results indicated that most PCGs were under negative selection.

Variation in the whole mitogenome of reef-building Porites corals

The study of complete mitochondrial genomes (mitogenomes) revealed different gene rearrangements, highly variable markers, and delineated clades that have aided the understanding of the evolutionary history in corals. In this study, we examined mitogenomic variation of reef-building Porites corals and designed 34 primer pairs to target high diversity regions and to amplify the complete mitogenome of a widely-distributed Indo-Pacific species of Porites (P. lobata) and two endemic species of the Eastern Pacific (P. sverdrupi and P. panamensis). All primer pairs amplified for each species and the mitogenomes assembled yielded the same gene order as obtained from next-generation sequencing. Mitogenomic variation in Porites corals was three to ten times higher than in Acropora or Pocillopora, two other major reef builders. In contrast to these corals, the nucleotide variation in Porites species was distributed evenly along the mitogenome. Primers designed here are useful to amplify regions with the highest variation possible as well as to assemble the whole mitogenomes of different Porites species. The resulting mitogenomes should improve our understanding of evolutionary relationships, delimitation of species, and conservation within the genus Porites.

Intraspecific Variation in Mitogenomes of Five Crassostrea Species Provides Insight into Oyster Diversification and Speciation.

A large number of Crassostrea oysters are found in Asia-Pacific. While analyses of interspecific variation have helped to establish historical relationships among these species, studies on intraspecific variation are necessary to understand their recent evolutionary history and current forces driving population biology. We resequenced 18 and analyzed 31 mitogenomes of five Crassostrea species from China: Crassostrea gigas, Crassostrea angulata, Crassostrea sikamea, Crassostrea ariakensis, and Crassostrea hongkongensis. Our analysis finds abundant insertions, deletions, and single-nucleotide polymorphisms in all species. Intraspecific variation varies greatly among species with polymorphic sites ranging from 54 to 293 and nucleotide diversity ranging from 0.00106 to 0.00683. In all measurements, C.hongkongensis that has the narrowest geographic distribution exhibits the least sequence diversity; C. ariakensis that has the widest distribution shows the highest diversity, and species with intermediate distribution show intermediate levels of diversity. Low sequence diversity in C.hongkongensis may reflect recent bottlenecks that are probably exacerbated by human transplantation. High diversity in C. ariakensis is likely due to divergence of northern and southern China populations that have been separated without gene flow. The significant differences in mitogenome diversity suggest that the five sister species of Crassostrea have experienced different evolutionary forces since their divergence. The recent divergence of two C. ariakensis populations and the C. gigas/angulata species complex provides evidence for continued diversification and speciation of Crassostrea species along China's coast, which are shaped by unknown mechanisms in a north-south divide.

The complete mitochondrial genome of the parthenogenetic Caucasian rock lizard Darevskia unisexualis (Squamata: lacertidae) contains long tandem repeat formed by 59 bp monomer

The first complete mitochondrial genome sequence of parthenogenetic Caucasian rock lizard Darevskia unisexualis (Lacertidae family) is determined by hybrid assembly with Illumina HiSeq and PacBio RS II platforms. The circular 21.4 kbp mitogenome contains 13 protein-coding genes, 12S and 16S rRNA genes, 20 tRNAs, two pseudogenized tRNAs, and one long tandem repeats with 4.1 kbp length formed by 59 bp monomer repeated x70.6 times located before control region. This finding represents a new example of mitogenome variation in lizards of hybrid origin, providing fundamental data for following study of a unique hybridization system formed by parthenogenetic and bisexual species in the mountain steppe of central Armenia.

Bayesian analyses of Yemeni mitochondrial genomes suggest multiple migration events with Africa and Western Eurasia.

Anatomically, modern humans are thought to have migrated out of Africa ∼60,000 years ago in the first successful global dispersal. This initial migration may have passed through Yemen, a region that has experienced multiple migrations events with Africa and Eurasia throughout human history. We use Bayesian phylogenetics to determine how ancient and recent migrations have shaped Yemeni mitogenomic variation. We sequenced 113 mitogenomes from multiple Yemeni regions with a focus on haplogroups M, N, and L3(xM,N) as these groups have the oldest evolutionary history outside of Africa. We performed Bayesian evolutionary analyses to generate time-measured phylogenies calibrated by Neanderthal and Denisovan mitogenomes in order to determine the age of Yemeni-specific clades. As defined by Yemeni monophyly, Yemeni in situ evolution is limited to the Holocene or latest Pleistocene (ages of clades in subhaplogroups L3b1a1a, L3h2, L3x1, M1a1f, M1a5, N1a1a3, and N1a3 range from 2 to 14 kya) and is often situated within broader Horn of Africa/southern Arabia in situ evolution (L3h2, L3x1, M1a1f, M1a5, and N1a1a3 ages range from 7 to 29 kya). Five subhaplogroups show no monophyly and are candidates for Holocene migration into Yemen (L0a2a2a, L3d1a1a, L3i2, M1a1b, and N1b1a). Yemeni mitogenomes are largely the product of Holocene migration, and subsequent in situ evolution, from Africa and western Eurasia. However, we hypothesize that recent population movements may obscure the genetic signature of more ancient migrations. Additional research, e.g., analyses of Yemeni nuclear genetic data, is needed to better reconstruct the complex population and migration histories associated with Out of Africa.

Mitogenomes from Egyptian Cattle Breeds: New Clues on the Origin of Haplogroup Q and the Early Spread of Bos taurus from the Near East.

BackgroundGenetic studies support the scenario that Bos taurus domestication occurred in the Near East during the Neolithic transition about 10 thousand years (ky) ago, with the likely exception of a minor secondary event in Italy. However, despite the proven effectiveness of whole mitochondrial genome data in providing valuable information concerning the origin of taurine cattle, until now no population surveys have been carried out at the level of mitogenomes in local breeds from the Near East or surrounding areas. Egypt is in close geographic and cultural proximity to the Near East, in particular the Nile Delta region, and was one of the first neighboring areas to adopt the Neolithic package. Thus, a survey of mitogenome variation of autochthonous taurine breeds from the Nile Delta region might provide new insights on the early spread of cattle rearing outside the Near East.MethodologyUsing Illumina high-throughput sequencing we characterized the mitogenomes from two cattle breeds, Menofi (N = 17) and Domiaty (N = 14), from the Nile Delta region. Phylogenetic and Bayesian analyses were subsequently performed.ConclusionsPhylogenetic analyses of the 31 mitogenomes confirmed the prevalence of haplogroup T1, similar to most African cattle breeds, but showed also high frequencies for haplogroups T2, T3 and Q1, and an extremely high haplotype diversity, while Bayesian skyline plots pointed to a main episode of population growth ~12.5 ky ago. Comparisons of Nile Delta mitogenomes with those from other geographic areas revealed that (i) most Egyptian mtDNAs are probably direct local derivatives from the founder domestic herds which first arrived from the Near East and the extent of gene flow from and towards the Nile Delta region was limited after the initial founding event(s); (ii) haplogroup Q1 was among these founders, thus proving that it underwent domestication in the Near East together with the founders of the T clades.

Mitogenomic variation of Bangladesh Penaeus monodon (Decapoda, Panaeidae) and reassessment of its phylogeography in the Indo-West Pacific region

Large variation in the mtDNA control region (CR) in Penaeus monodon has been reported from the Indo-West Pacific region, characterizing three distinct lineages, A, B and C. This diversification has been explained by geographic barriers but may also be due to paralogous duplication events. Here we evaluate the diversity, origin and population patterns of this species in Bangladesh based on mtDNA, and reconsider the evidence for paralogous duplication. MtDNA variation revealed high diversity with almost all individuals carrying a unique haplotype, indicating a large effective population size and a single reproductive pool. The Bangladesh haplotypes cluster within lineage C, found mainly west of the Sunda Shelf. This lineage, which diverged from lineages A and B around 6.6 Mya, has diverged further into several lineages in the western Indian Ocean. Sequences of mitochondrial CR, 16S rRNA gene and a combined fragment of the 16S rRNA and tRNAVal genes from Bangladesh did not reveal any duplication or heteroplasmy. Further, phylogenies based on the three markers, including samples from different areas in the Indo-West Pacific region, support the occurrence of three distinct lineages. Thus, the variation in CR appears to result from segregation of orthologous variants rather than diversification following a paralogous duplication.

Characterization of the complete mitochondrial genome of the Rhinolophus sinicus sinicus (Chiroptera: Rhinolophidae) from Central China

We present a complete mitochondrial genome sequence of Rhinolophus sinicus sinicus from Central China and provide its annotation, as well as showed the phylogenetic relationship and mitogenomic variation with other published mitochondrial genomes of congeneric bat species. Our results revealed a relatively high mitogenomic variation between two R. s. sinucus from Central and East China, which is similar to interspecific divergence level.

Improved characterisation of among-lineage rate variation in cetacean mitogenomes using codon-partitioned relaxed clocks

Background and aims. There is extensive variation in substitution rates among metazoan mitochondrial genomes, including differences among lineages and among sites. Differences in substitution rates among lineages are routinely taken into account in molecular phylogenetic and dating analyses. However, this is rarely the case for differences in the lineage-specific patterns of rate variation among sites.Materials and methods. We analysed an alignment of 32 cetacean mitogenomes using a partitioned relaxed-clock approach, in which a separate relaxed-clock model was applied to each of the three codon positions of the protein-coding genes.Results. By comparing Bayes factors, we found overwhelming support for this model compared with a strict-clock model and less-complex models comprising fewer relaxed clocks. Our analyses reveal the presence of substantial rate heterogeneity among cetacean lineages, and that these patterns of variation differ between codon positions. However, we find no evidence of mitochondrial rate autocorrelation throughout the cetacean phylogeny.Conclusions. Our study confirms the feasibility of applying a partitioned relaxed-clock model to mitogenomic data, and suggests that molecular phylogenetic and dating analyses may be improved by the application of these models.