Skip to content

Advertisement

  • Research
  • Open Access

Evolution of mitochondrial genomes in Baikalian amphipods

  • 1,
  • 2, 3,
  • 1,
  • 2, 3,
  • 2, 3, 4,
  • 1,
  • 5,
  • 5 and
  • 1, 6Email author
BMC Genomics201617 (Suppl 14) :1016

https://doi.org/10.1186/s12864-016-3357-z

  • Published:

Abstract

Background

Amphipods (Crustacea) of Lake Baikal are a very numerous and diverse group of invertebrates generally believed to have originated by adaptive radiation. The evolutionary history and phylogenetic relationships in Baikalian amphipods still remain poorly understood. Sequencing of mitochondrial genomes is a relatively feasible way for obtaining a set of gene sequences suitable for robust phylogenetic inferences. The architecture of mitochondrial genomes also may provide additional information on the mechanisms of evolution of amphipods in Lake Baikal.

Results

Three complete and four nearly complete mitochondrial genomes of Baikalian amphipods were obtained by high-throughput sequencing using the Illumina platform. A phylogenetic inference based on the nucleotide sequences of all mitochondrial protein coding genes revealed the Baikalian species to be a monophyletic group relative to the nearest non-Baikalian species with a completely sequenced mitochondrial genome - Gammarus duebeni. The phylogeny of Baikalian amphipods also suggests that the shallow-water species Eulimnogammarus has likely evolved from a deep-water ancestor, however many other species have to be added to the analysis to test this hypothesis.

The gene order in all mitochondrial genomes of studied Baikalian amphipods differs from the pancrustacean ground pattern. Mitochondrial genomes of four species possess 23 tRNA genes, and in three genomes the extra tRNA gene copies have likely undergone remolding. Widely varying lengths of putative control regions and other intergenic spacers are typical for the mitochondrial genomes of Baikalian amphipods.

Conclusions

The mitochondrial genomes of Baikalian amphipods display varying organization suggesting an intense rearrangement process during their evolution. Comparison of complete mitochondrial genomes is a potent approach for studying the amphipod evolution in Lake Baikal.

Keywords

  • Mitochondrial Genome
  • tRNA Gene
  • Complete Mitochondrial Genome
  • Mitochondrial Genome Sequence
  • Amphipod Species

Background

Ancient freshwater lakes are the birthplaces of very diverse and mostly endemic biota. Their eco-systems are «natural laboratories of evolution» that offer insights into many evolutionary topics, attracting continuous attention of the scientific community and advancing the elucidation of the speciation mechanisms [1, 2]. About ten of the contemporary freshwater lakes existed for longer than one million years. Among them, Lake Baikal is the oldest (reviewed in [14]). The age of Lake Baikal is estimated by different authors to be in the range of 25 to 30 million years [5, 6].

Similarly to other ancient giant lakes, a greater part of the huge diversity of animals inhabiting Lake Baikal belongs to the species flocks [7]. These diverse groups of monophyletic species are believed to evolve in the confines of the lake through adaptive radiation in sympatry [2, 8, 9], although geographic isolation is possible in some cases [1012].

Amphipods are the most diverse group of Baikalian invertebrates (more than 350 described species). They are extremely diverse morphologically and have a wide range of ecological specificities [13, 14].

Most of Baikalian amphipod species have evolved in the confines of Lake Baikal, although some of them have later spread to other water bodies in Eurasia [13, 14]. The only Holarctic species inhabiting shallow bays of Lake Baikal is Gammarus lacustris Sars, 1864 [14, 15]. Also Gammarus dabanus Takhteev et Mekhanikova, 2000, an endemic species from the mountain streams of Khamar-Daban ridge, was found at the edge of Baikal near the estuaries [16]. The discovery and description of all amphipod species from Lake Baikal is still far from approaching completion (i.e. [12, 1619]). The work on the revision of their higher level taxonomy is still in progress [13, 14, 17, 1927]. According to the most modern revision by Kamaltynov [17] all Baikalian amphipod species belong to 76 genera and eleven families, ten of which are autochthonous: Carinogammaridae Tachteev, 2000, Crypturopodidae Kamaltynov, 2001, Macrohectopodidae Sowinsky, 1915, Micruropodidae Kamaltynov, 1999, Baikalogammaridae Kamaltynov, 2001, Ommatogammaridae Kamaltynov, 2009, Acanthogammaridae Garjajeff, 1901, Eulimnogammaridae Kamaltynov, 1999, Pachyschesidae Kamaltynov, 1999, Pallaseidae Tachteev, 2001.

Application of molecular phylogenetic approaches allowed to refine the taxonomy of Baikalian amphipods and to outline the main trends of their evolution, specifically their phylogenetic position relative to the non-Baikalian amphipod taxa. It was shown that at the very beginning of the diversification Baikalian amphipods had split into at least two major lineages delineated by their ecological and morphological traits [2832]. This observation could also be explained by two independent colonizations of Lake Baikal. Several groups have shown that the ancestors of the extant Baikalian amphipods were closely related to the ancestors of the Holarctic species of Gammarus Fabricius, 1775 [28, 3034].

Englisch et al. (2003) showed that Baikalian species Parapallasea lagowskii (Dybowsky, 1874) was «nested within genus Gammarus» [33]. In the study by McDonald et al. performed on 32 species of Baikalian amphipods and 29 non-Baikalian species only species belonging to the family Micruropodidae clustered together with Gammarus [30]. An early study by Sherbakov et al. based on partial 18S rRNA sequences showed close relationship of the two Baikalian lineages to different species of Gammarus [28]. This was later confirmed in the detailed study by Hou and Sket, which utilized more genetic markers and sampled more species of Gammaridae [32]. One lineage of Baikalian amphipods was found to be a sister group to the “Oriental Gammarus clade”, the other one was closer to the “Eurasian clade” [32]. Molecular phylogeny also revealed inconsistencies in the current taxonomy of Baikalian amphipods. Genera Acanthogammarus Stebbing, 1899 and Pallasea Bate, 1862 were shown to be polyphyletic [11, 28, 35].

Majority of the previous molecular studies of evolutionary history and taxonomy of Baikalian amphipods are impeded by insufficient statistical support of the most important clades [28, 30, 35, 36]. The presence of poorly resolved clades might be explained both by insufficient length of sequences used and by their low mutational rate (e.g.18S rDNA) [29, 35]. Unfortunately, more recent works aimed at resolving the complicated relations within Gammarus included only a few Baikalian species or did not address their phylogenetic relationship [31, 32, 37, 38]. Therefore, further study of Baikalian amphipods is necessary to elucidate their phylogeny.

In this study we use nucleotide sequences of completely sequenced mitochondrial genomes (mitogenomes) for the evolutionary inferences and clarification of the taxonomy of Baikalian amphipods. The ten studied species appear to form a single clade relative to Gammarus duebeni Lilljeborg, 1852. We also perform a detailed comparative structural analysis of amphipods mitochondrial genomes and find an unexpectedly high degree of their length variation and extensive gene rearrangements.

Results and Discussion

Mitochondrial genomes organization

We obtained three complete and four nearly complete sequences of mitochondrial genomes from Baikalian amphipod species. Information about animals sampling sites, sequences lengths, numbers of reads, GenBank accession numbers, etc. of currently studied Baikalian amphipod species and that of previously published ones is presented in Table 1. Acanthogammarus victorii (Dybowsky, 1874) and Garjajewia cabanisii (Dybowsky, 1874) have incomplete non-coding regions sequences due to their low complexity and the presence of repeats (the 51-mer tandem repeats in the control region (CR) of A. victorii and the CR sequence duplication in the mitochondrial genome of G. cabanisii) that have prevented automatic assembly process. Mitochondrial genomes of Crypturopus tuberculatus (Dybowsky, 1874) and Linevichella vortex (Dybowsky, 1874) also lack various parts of the coding sequences due to the difficulties in amplification of these regions. The sizes of complete mitochondrial genomes range from 14,370 to 18,114 b.p., which is within the range of mitogenomes of other amphipods (14,113 to 18,424 b.p.). The AT content varies from 62.24 to 68.96% for completely sequenced mitochondrial genomes and from 57.45 to 64.86% for partially sequenced ones (Table 2). In general this is compatible with the values of other known complete amphipod mitogenomes (64.03–76.03%), although the AT content of Brachyuropus grewingkii (62.24%) was found to be the lowest within amphipods [3947].
Table 1

Summary of the Baikalian amphipod data presented in the study

Species

Sampling site, coordinates

Ecological features: depth of habitat, armament, nutrition

DNA template type, number of paired reads

Mean coverage of mitogenome

Mitogenome size, b.p.

AT-skew

GC-skew

GenBank nos.

References

Acanthogammarus victorii

Listvyanka,

51°51’30” N,

104°50’37” E

1.5–90 m., spiny, predator/scavanger

total DNA,

6.3 M

40×

17,424 a

0.027

−0.251

KX341962

This study

Brachyuropus grewingkii

Estuary of Buguldeyka river, 52°28’N,

106°06’E–52°28’N, 106°05’E

100–1380 m., (usually deeper than 300 m.) spiny, predator

total DNA,

6.4 M

12×

17,118

0.003

−0.307

KP161875

[105]

Crypturopus tuberculatus

Estuary of Anga river, 52°46’40” N, 106°34’60” E

1.5–99 m., tuberous, detritophagous

mitochondrial DNA amplicons, 59,961

901×

13,864 b

−0.070

−0.013

KX341963

This study

Eulimnogammarus cyaneus

Sukhoi Ruchey, 51°38’48” N, 103°45’14” E

0–3.5 m., smooth,

phytophagous

mitochondrial DNA amplicons, 541,283

7665×

14,370

−0.019

−0.251

KX341964

This study

Eulimnogammarus verrucosus

Bol’shie Koty, 51°54’11.67” N, 105°04’07.61” E

0–12 m., (usually 0–3 m.) smooth, phytophagous

total DNA,

352.7 M

1000×

15,314

−0.007

−0.238

KF690638

[71]

Eulimnogammarus vittatus

Sukhoi Ruchey, 51°38’ 48” N, 103°45’14” E

0–30 m., (usually 0–3 m.) smooth, phytophagous

total DNA,

4.6 M

21×

15,534

−0.014

−0.222

KM287572

[104]

Garjajewia cabanisii

Estuary of Buguldeyka river, 52°28’N, 106°06’E–52°28’N, 106°05’E

80–1250 m., (usually deeper than 200 m.) spiny, predator

total DNA,

7.5 M

24×

17,576 a

−0.002

−0.286

KX341965

This study

Gmelinoides fasciatus

Sukhoi Ruchey, 51°38’ 31” N, 103°46’ 03” E

0–192 m. (usually 0–5 m.), tuberous, phytophagous/

euryphagous

total DNA,

7.4 M

14×

18,114

−0.001

−0.303

KX341966

This study

Linevichella vortex

Listvyanka,

51°51’12” N, 104°51’48” E

0–88 m., (usually 1–2 m.) smooth, phytophagous

mitochondrial DNA amplicons, 13,319

132×

11,444 b

−0.027

−0.223

KX341967

This study

Pallaseopsis kesslerii

Estuary of Anga river, 52°46’40” N, 106°34’60” E

1–61 m., slightly spiny, phytophagous

mitochondrial DNA amplicons, 14,144

154×

15,759

0.010

−0.182

KX341968

This study

Bold numbers indicate incomplete sequences

aa mitochondrial genome with an incomplete non-coding part

ba mitochondrial genome with incomplete sequences of both coding and non-coding parts

M denotes million reads

Table 2

Comparison of mitogenomic characteristics of Baikalian amphipods

Species

Genome

PCGs

rRNAs

tRNAs

Putative CRs

Intergenic spacers

Length, b.p.

AT %

Length, b.p.

AT %

Length, b.p.

AT %

Length, b.p.

AT %

Length, b.p.

AT %

Length, b.p.

AT %

Acanthogammarus victorii

17,424

59.28

11,043

57.01

1616

63.68

1360

64.34

1390

70.86

2035

56.86

Brachyuropus grewingkii

17,118

62.24

11,056

60.20

1608

66.36

1304

65.41

1264

73.26

1852

61.56

Crypturopus tuberculatus

13,864

57.45

10,803

56.53

798

63.28

1078

62.15

-

-

1207

57.91

Eulimnogammarus cyaneus

14,370

67.59

11,047

66.78

1607

71.81

1300

66.69

181

77.90

268

75.37

Eulimnogammarus verrucosus

15,314

68.96

11,022

66.63

1602

69.54

1335

67.42

437

83.30

872

76.63

Eulimnogammarus vittatus

15,534

67.42

11,050

65.59

1606

71.30

1373

67.30

1053

79.01

491

72.51

Garjajewia cabanisii

17,576

64.86

11,052

62.67

1605

66.98

1367

65.47

1212

76.07

2324

67.60

Gmelinoides fasciatus

18,114

65.87

11,448

63.29

1594

69.01

1348

66.47

235

81.28

3863

70.88

Linevichella vortex

11,444

64.51

9813

64.15

538

67.84

829

64.29

-

-

296

72.97

Pallaseopsis kesslerii

15,759

63.10

11,035

61.13

1597

64.87

1361

67.52

340

80.59

1800

70.67

Bold numbers indicate incomplete sequences

All completely sequenced mitochondrial genomes of Baikalian amphipods have strong negative values of GC-skew (prevalence of C over G) on the (+) strand (−0.30 to −0.18) and their AT-skew (prevalence of A over T) varies from −0.02 to 0.01 (Table 1, Additional files 1 and 2). Species with partial mitochondrial genome sequences have GC-skew from −0.25 to −0.01 and AT-skew from −0.07 to +0.02. The unequal nucleotide content between two strands is typical for mitochondrial DNA. This is a consequence of an asymmetric mutational process that affects the A and C nucleotides during the replication and transcription [48, 49].

Complete sequences of Baikalian amphipod mitochondrial genomes contain 13 protein coding genes, two rRNA genes and from 22 to 23 tRNA genes, a CR and intergenic spacers of different number and lengths (Fig. 1, annotations of studied mitochondrial genomes are in Additional file 3).
Fig. 1
Fig. 1

Organization of mitochondrial genomes of Baikalian amphipods in comparison to the pancrustacean ground pattern. Genes on the (+) strand are located above the line, whereas genes coded on the (−) strand are below the line. Transfer RNAs genes are labeled by their single-letter amino acid code. Oblique strokes in some genomes denote unknown areas that were not sequenced due to technical difficulties. Gene features with altered location in comparison to the pancrustacean ground pattern are shown in grey color. Location of a putative CR sequence of B.grewingkii has been changed from the one inferred in the previously published article by Romanova et al. [105]

Protein-coding genes order

All completely sequenced Baikalian amphipod mitochondrial genomes possess a typical set of 13 protein-coding genes (PCGs). PCGs of each species have the same transcriptional polarity as in the pancrustacean ground pattern [50] (Fig. 1), however the order of PCGs has been altered relative to the ground pattern in the mitochondrial genomes of three species under study. Pallaseopsis kesslerii (Dybowsky, 1874) has a translocation of the nad1 gene, C. tuberculatus possesses translocation of nad5, cytB, nad1, cox3, nad3, nad4, nad4l, nad6, Gmelinoides fasciatus (Stebbing, 1899) has translocations of nad1, nad5, nad4, nad4l, nad6 and cytB (Fig. 1). These re arrangements have never been observed in other amphipod species.

The only feature in common among the amphipods with the altered gene order is that they are relatively shallow water dwellers (Table 1) belonging to the Micruropus flock [35]. However, there are other shallow water amphipods in the dataset which have an unaltered order of mitochondrial genes.

In the non-Baikalian amphipods one may also find deviations from the pancrustacean ground pattern. Onisimus nanseni G.O. Sars, 1900 has nad6 and cytB translocation, in some species of Metacrangonyx Chevreux, 1909 cytB is inverted [39, 40, 45], the species of Caprella Lamarck, 1801 have nad4, nad4l, nad6 translocations and nad5 inversion. Gene order in the species belonging to Pseudoniphargus Chevreux, 1901 differs from the pancrustacean ground pattern and is variable within the genus. P. daviui Jaume, 1991 has nad1 translocation and P.sorbasiensis Notenboom, 1987 has nad6, cytB translocation.

Non-Baikalian amphipods with rearranged PCGs relative to the pancrustacean ground pattern are distant from each other taxonomically (up to a superfamily level) as well as ecologically. Among the species with an altered gene order there are two genera of freshwater stygobionts: Palearctic genus Metacrangonyx (superfamily Hadzioidea) and Nearctic genus Pseudoniphargus (superfamily Allocrangonyctoidea) [34], Arctic marine species O.nanseni (superfamily Lysianassoidea) [42] and some species of Caprella (superfamily Caprelloidea) inhabiting warm seas around the world [51, 52]. Still, amphipods carrying the unchanged ground pattern are at least equally taxonomically and ecologically diverse. Parhyale hawaiiensis (Dana, 1853) (superfamily Talitroidea) is a marine species distributed in north Atlantic [53], Bahadzia jaraguensis Jaume and Wagner, 1998 (superfamily Hadzioidea) is a stygobiontic species that was found in the caves of West Indian and Caribbean regions [54, 55], G. duebeni (superfamily Gammaroidea) is a North Atlantic distributed species [56], Gondogeneia antarctica (Chevreux, 1906) (superfamily Calliopioidea) is a South Antarctic species [57].

It seems that the changes in the gene order of Baikalian as well as non-Baikalian amphipods can not be directly correlated with any meaningful environmental parameter. Similarly, although it is possible that some lineages are more prone to reshuffling of their mitochondrial genes then the others, they do not appear to be phylogenetically clustered. Obviously, further careful investigation with a more comprehensive dataset is necessary to resolve the ancestral pattern of Baikalian amphipod mitochondrial genomes.

Base composition bias in protein-coding genes

The GC-skew values were measured for all protein coding genes similarly to the measure of strand composition bias [58]. Mitochondrial genomes of most Baikalian amphipod species studied here have negative GC-skew in PCGs that are located on the (+) strand. PCGs encoded on the (−) strand, on the contrary, have positive GC-skew (Fig. 2, Additional file 2). Such strand bias is typical for most mitochondrial genomes in Malacostraca [42, 59]. However, in C. tuberculatus, the composition bias was found to be noticeably lower than in the other species. The GC-skew values of the (+) strand PCGs vary from −0.11 to +0.14 and of the (−) strand PCGs GC-skew values vary from +0.02 to +0.09 (Fig. 2). In the nad3 and nad6 genes the strand bias is reversed and thus the GC-skew is positive.
Fig. 2
Fig. 2

Statistical data for PCGs and ribosomal genes in mitochondrial genomes of Baikalian amphipods. a GC-skew values of PCGs and ribosomal genes. (+) marks genes coded by the positive strand, (−) marks genes coded by the negative strand. b An illustration of a positive correlation between the effective number of codons (ENC) and the GC content at the third codon position (GC3s) in Baikalian amphipods. c Nucleotide diversity (Pi) values for PCGs of Baikalian and non-Baikalian amphipods. d AT content (%) in three codon positions in PCSs of Baikalian amphipods

The strand bias reversion was previously detected in the mitochondrial genomes of several different invertebrate species such as Katharina tunicata (Mollusca), Florometra serratissima (Echinodermata), Argiope amoena (Chelicerata), Aleurochiton aceris, Bemisia tabaci, Campanulotes bidentatus, Thrips imaginis, Bothriometopus macrocnemis, Cotesia vestalis, Neomaskellia andropogonis, Tetraleurodes acacia ect. (Hexapoda), Ligia oceanica, Hutchinsoniella macracantha, Tigriopus californicus, Lepeophtheirus salmonis, Calanus hyperboreus, Argulus americanus, Procambarus clarkii, Corallianassa couitierei, Nihonotrypaea japonica, Cambaroides similis, Homarus gammarus ect. (Crustacea) [43, 45, 49, 58]. Within amphipods the reversed strand bias was found in the mitochondrial genomes of Metacrangonyctidae species [45]. As previously suggested by Hassanin et al., 2005, the strand reversion can happen due to the reversion of one or several genes relative to the CR or alternatively, it could be explained by the reversion that includes the CR [49]. We did not succeed in sequencing the CR of C. tuberculatus and thus we can not conclude which scenario is more likely in this case. Still, taking into account the relatively low values of GC skew of the majority of protein coding mitochondrial genes in this organism, one may speculate that the reversion is a relatively recent event on the evolutionary time scale [49]. Taxa with a reversed strand bias should be taken into phylogenetic analysis with caution as they tend to promote long branch attraction artifacts [49].

AT content in protein-coding genes and codon usage

The AT content of completely sequenced PCGs varies from 57.01% (in A.victorii) to 66.78% (in Eulimnogammarus cyaneus (Dybowsky, 1874)) (Table 2). The PCGs of A. victorii have the lowest AT content among entirely sequenced mitochondrial genomes of amphipods. Codon positions in mitochondrial PCGs were noted to have an unequal AT content. Mitochondrial genomes studied here have the lowest AT content at the first codon position, a slightly higher AT content at the second position and the highest AT content at the third codon position (Fig. 2). The A. victorii and C.tuberculatus species, however, have the highest AT content at the second codon position in their PCGs, and the lowest at the first codon position (Fig. 2).

Codon usage analysis in Baikalian amphipods revealed the presence of all codon types typical for the invertebrate mitochondrial code (Additional file 4). Along with the regular start codons (ATA and ATG), the unusual ones (ATT, ATC, TTG and GTG) were predicted to initiate mitochondrial PCGs. Presence of unusual start and stop codons is generally typical for mitochondrial genomes [60]. Some PCGs of the investigated genomes possess truncated stop codons (T) that are presumably completed after a post-transcriptional polyadenylation [61] (Additional file 3).

In all currently studied genomes the most frequently used codons are TTT (Phe) (5.40 to 7.05%) and TTA (Leu) (4.69 to 8.72%). Also some of the more frequent codons include ATT (Ile) (2.93 to 5.54%), ATA (Met) (3.69 to 6.07%) (Additional file 4). In non-Baikalian amphipods these four codons are also among the most abundant ones. Bias toward the AT-rich codons is typical for many arthropods [62].

The Effective Number of Codons (ENC) [63] in Baikalian amphipods varies widely, ranging from 45.04 in Eulimnogammarus verrucosus (Gerstfeldt, 1858) to 55.67 in C.tuberculatus (Fig. 2). These values exceed slightly the ENC in other amphipod species, which range from 36.47 to 49.74. A strong positive correlation (r = 0.97) between ENC and GC content at the third codon position was found in mitochondrial genomes of Baikalian amphipods (Fig. 2). The ENC in all sequenced genomes increases with the decrease of AT content in protein coding genes.

Nucleotide diversity analysis

Nucleotide diversity (Pi) was estimated for two groups of protein-coding genes, the first one encompasses the Baikalian amphipod species, the second one contains non-Baikalian species (see species list in Additional file 5) (Fig. 2). These data may be useful for designing new molecular markers for phylogenetic inferences of amphipods. The patterns of nucleotide diversity within mitochondrial genes in both groups were nearly identical, with lower values for genes of Baikalian amphipods. This may be due to the much higher evolutionary span of the non-Baikalian amphipod species in comparison to the Baikalian amphipods. Indeed, all Baikalian amphipods belong to a single superfamily Gammaroidea, while the rest of analyzed amphipods represent superfamilies Hadzioidea, Allocrangonyctoidea, Lysianassoidea, Caprelloidea, Talitroidea, Gammaroidea, Calliopioidea.

In both groups the cox1 sequences have the smallest values of diversity (0.23 ± 0.01 for Baikalian species, and 0.24 ± 0.01 for non-Baikalian ones), whereas the atp8 appears to be the most variable (0.43 ± 0.03 for Baikalian species and 0.47 ± 0.01 for non-Baikalian ones) (Fig. 2). The highest difference in the nucleotide diversity between Baikalian and non-Baikalian species was noted in the nad6, which might be caused by the lack of a complete sequence from L.vortex. Other studies dedicated to animal mitochondrial genomes also revealed the cox genes to be the most conserved and the atp genes to be the most variable [45, 6468]. However, there are animal groups with the different patterns of nucleotide variability distribution within protein coding genes of their mitochondrial genomes [69, 70]. It seems that the pattern of nucleotide diversity is a lineage specific feature.

On the basis of the data of all available Baikalian amphipod mitochondrial genomes it is possible to predict which genes are more suitable for different phylogenetic applications in this taxonomic group. The most variable genes (atp8, nad2, nad4l, nad5, nad6) can be utilized as markers for species level phylogeny and population studies. Alternatively, sequences of the least variable mitochondrial cox genes may be suitable for deep phylogeny (families and higher taxa) investigations.

Transfer RNA genes

From 22 to 23 tRNA genes were identified in the completely sequenced mitogenomes of Baikalian amphipod species. The locations of tRNA genes are highly variable and all studied mitochondrial genomes have tRNA genes with altered positions relative to the pancrustacean ground pattern (Fig. 1).

The secondary structures of 213 mitogenome-encoded tRNAs ranging from 49 to 64 b.p. in length and including those of E.verrucosus [71] were predicted for the analysis (Additional file 6). Most of the predicted tRNAs possess the expected clover-leaf structures, however some of them have aberrant structures. The tRNA-Ser (UCU) lacks the DHU arm in all studied species. The DHU arm is also missing in the tRNA-Val of B.grewingkii, A.victorii, E.cyaneus, and G.cabanisii, in the tRNA-Ser (UGA) of G.fasciatus and L.vortex, and in the tRNA-Tyr of G.fasciatus. The tRNA-Gln lacks the TψC arm in all studied species except for C.tuberculatus. The TψC arm is also absent in the tRNA-Thr of G.fasciatus and in the tRNA-His and tRNA-Pro of P.kesslerii (Additional file 6).

The presence of tRNAs with aberrant structures was found to be typical for crustaceans [39, 4145, 47, 7276] and can also be seen in other invertebrates [77, 78]. The presence of aberrant tRNAs in mitochondrial genomes is usually explained either by selection towards minimization of the mitochondrial genome [77] or by replication slippage [79].

In four out of ten studied mitogenomes the additional tRNA gene copies are found along with the standard set of 22 tRNA genes. A copy of trnP is found in Eulimnogammarus vittatus (Dybowsky, 1874), trnL1 in G.cabanisii, trnQ in G. fasciatus and trnD in A. victorii (Fig. 1, Additional files 3 and 6). The copies of tRNA-Pro, tRNA-Leu1 and tRNA-Asp possess the standard clover-leaf structure. In G. fasciatus a clover-leaf structure is seen in one tRNA-Gln copy (Q2), whereas the other copy (Q1) lacks the TψC arm (Additional file 6). P.kesslerii also has an additional tRNA adhering to a typical clover-leaf structure, which however has four bases at the presumed anticodon site. The nucleotides in the middle of the anticodon loop may correspond to either Phe or Ile depending on the exact position of the anticodon. An abnormal anticodon suggests that this copy is a pseudogene (ψ F/I) (Additional file 6).

The presence of additional tRNA genes was noted in many mitochondrial genomes of both vertebrate and invertebrate species. If the duplications occurred recently both copies are either identical or very similar in the primary sequence [8083]. The copies maintain functionality if they retain some conserved elements of their secondary structure [84]. One of the two copies may subsequently undergo elimination. The vestiges of such copies that accumulated substitutions are identified as pseudogenes [85, 86]. Another possible mechanism involves the switch of tRNA identity as the consequence of a point mutation in the anticodon. This mechanism was called tRNA remolding by Cantatore et al. [87].

While the trnL1 genes of G.cabanisii share 75.00% identity pointing to their origin from a single trnL1 gene, the tRNA duplicates in other amphipods may have switched their identities: one of the two trnP genes in E. vittatus has 78.68% identity with the trnL1, in G. fasciatus a copy of trnQ has 70.00% identity with the trnH gene, and in A. victorii a copy of trnD gene has 67.21% identity with the trnH gene. It is likely that the additional tRNA genes of E. vittatus, G. fasciatus and A. victorii have been undergone remolding.

Evidence of tRNA remolding was found in mitochondrial genomes of different groups, including Porifera [8891], Mollusca [92, 93], Echinodermata [87], Arthropoda [43, 91], Chordata [94, 95]. It was recently shown that the remolding event of Trp (UCA) to Gly (UCC) took place in the ancestor of amphipods [91]. Additional tRNA copies found in the mitogenomes of Baikalian amphipods illustrate different stages of the rearrangement process.

Ribosomal RNA genes

The rRNA genes in mitochondrial genomes of all studied amphipods are located on the (−) strand. In two out of eight mitochondrial genomes with the completely sequenced coding portion (G.fasciatus and P.kesslerii) the rRNA genes have altered positions in comparison to the pancrustacean ground pattern [50] (Fig. 1, Additional file 3). Rearrangements in the mitochondrial genome involving ribosomal RNA genes or/and PCGs occur much less frequently than those involving only tRNA-coding genes [9698], thus they are called «major rearrangements» [98]. The rearrangements of rRNA genes and PCGs might potentially affect the effectiveness of replication and transcription of mitochondrial genomes.

The length of completely sequenced Baikalian amphipods’ rrnL genes varies from 976 to 984 b.p., and the rrnS gene length varies from 618 to 630 b.p. (Additional file 7). The lengths of rRNA genes in Baikalian amphipods appear to be slightly smaller than those in previously sequenced amphipod mitochondrial genomes [4042, 4447]. The AT content ranges from 64.50 to 73.75% in the rrnL genes, and from 62.38 to 70.90% in the rrnS genes respectively (Additional file 7). The GC-skew calculations for rRNA genes give highly positive values (from 0.23 to 0.39 for completely sequenced genes) that are comparable to the values calculated for PCGs encoded on the (−) strand (Additional file 7).

Control region and intergenic spacers

Mitochondrial genomes of Baikalian amphipods have varying numbers and lengths of non-coding regions (Additional file 3). Control region (CR) is the most important non-coding part involved in replication and transcription of the mitochondrial DNA [99]. For identification of a putative CR we searched features typically associated with such regions in invertebrates (poly-T stretch, tandemly repeated sequences, hairpin structures, AT-rich sequences (Additional file 1) [49, 58, 99103].

In the mitochondrial genome of E. cyaneus a putative CR is a 181 b.p sequence between the rrnS gene and the trnY-trnQ-trnC-trnI-trnM-nad2 gene cluster. A similar CR location was also observed in the previously published mitochondrial genomes of E.vittatus (1053 b.p.) [104] and E.verrucosus (473 b.p.) [71] and also in the mitochondrial genome of G. duebeni [44] (Fig. 1, Additional file 3).

Mitochondrial genomes of A.victorii and B.grewingkii [105] possess large non-coding sequences between the rrnS and nad2 genes. These sequences are interrupted by several tRNA genes. A putative CR in A.victorii is located between the locus containing a 13-T stretch and the trnI gene. This region was not sequenced completely, however all features typical for a CR were found in the partial sequence of the 1390 b.p. long locus. A putative CR in B.grewingkii is a 1264 b.p. long stretch between the 11-T locus and the trnD gene (Fig. 1, Additional file 3).

In the mitochondrial genome of G.cabanisii the CR is located between the rrnS gene and one of the duplicated trnL1 (trnL1/1) and measures 1212 b.p. in length. (Fig. 1, Additional file 3). Additionally we found traces of a second CR-like sequence located between the nad2 gene and the trnL1/2-rrnL-trnV-rrnS gene cluster. This region was not sequenced in its entirety, only the regions of 102 b.p. and 232 b.p. corresponding to its flanks were sequenced. The 102 b.p. region has a 98.03% identity with the corresponding region of the original CR, whereas the 232 b.p. region has a 65.60% identity with the other flank of the original CR (Additional file 8). It is likely that the latter region has undergone degeneration after the duplication. Without the complete sequence it is difficult to estimate the time of duplication and the exact sequence of events that led to the appearance of the second CR or speculate about its possible function. Thus we annotated these sequences simply as non-coding regions. The CR duplications were observed in mitochondrial genomes of some invertebrates, including ticks [106, 107], ostracods [108], sea cucumbers [109], katydids etc. [110]. Amphipods Caprella mutica Schurin, 1935 and Caprella scaura Templeton, 1836 also possess highly identical duplicated CRs in their mitochondrial genomes [41, 43].

The position of CR between the rrnS and nad2 genes in the mitochondrial genomes is typical for some other amphipods: G. duebeni [44], O. nanseni [42], G. antarctica [46], several species of Pseudoniphargus [47] and for the pancrustacean ground pattern as well [50], although the adjacent tRNA genes are often different.

The mitochondrial genome of P.kesslerii has a large non-coding sequence between the nad1 and nad2 genes that is separated by a few tRNA genes and one pseudo tRNA gene. A 340 b.p. sequence located between the 10-T locus and the pseudo tRNA gene (ψ F/I) was defined as a CR (Fig. 1, Additional file 3).

The mitochondrial genome of G. fasciatus possesses two large non-coding regions: one between the rrnS and nad5 genes, the other between the nad5 and nad4 genes. Both of these regions are interrupted with several tRNA genes. A 235 b.p. region between the rrnS and trnV was identified as a CR. All other non-coding regions were annotated as intergenic spacers (Fig. 1, Additional file 3).

It is notable that while most features typical for the CRs are found in the corresponding regions in the majority of sequenced mitochondrial genomes of Baikalian amphipods, the mitogenomes of E. cyaneus and A.victorii only possess tandem repeats.

Variation in the CR location was found in other amphipod species with an altered protein-coding and ribosomal RNA gene order. In the mitochondrial genomes of species from the Metacrangonyx genus the CR sequences were identified between the rrnS and cytB genes [39, 40, 45]. In C. mutica and C. scaura [41, 43] the first CR is located between the nad6 gene and the trnC-cytB gene cluster, and the second CR is located between the nad4l-trnP and the trnI-trnM-trnY-trnQ-nad2 gene clusters. The lengths of CR sequences in non-Baikalian amphipods also vary significantly from 25 b.p. in M. goulmimensis to 1626 b.p. in G. duebeni [4042, 4447]. Furthermore, it was previously shown that this feature varies considerably even between individuals of the same species. Such CR length variation was noted in Metacrangonyx longipes Chevreux, 1909 (26 and 40 b.p.) and Metacrangonyx goulmimensis Messouli, Boutin and Coineau, 1991 (25 and 471 b.p.) [40, 45]. Thus, the variable location and length of CR sequences in mitochondrial genomes of the Baikalian amphipod species is in concordance with the characteristics of CRs in other amphipods and invertebrates in general.

The number of intergenic spacers in completely sequenced mitochondrial genomes of Baikalian amphipods varies from 9 to 21 and their total length varies from 268 to 3863 b.p. (Table 2, Additional file 3). Three Baikalian amphipods with entirely sequenced mitochondrial genomes (B.grewingkii, P.kesslerii, and G.fasciatus) possess the largest portions of intergenic spacers which take up 10.80, 11.42, and 21.32% of their complete mitochondrial genomes length. Within the currently sequenced non-Baikalian amphipods only G. antarctica [46] has a comparable length of the non-coding intergenic spacers (4354 b.p. in total). The presence of large and numerous intergenic spacers in some mitochondrial genomes studied here may be an evidence of former duplication events [111].

Distinct features of Baikalian amphipod mitochondrial genomes

Structural analysis of Baikalian amphipod mitochondrial genomes identified several features that differ in most of the studied mitogenomes. Alterations in gene order, strand bias reversion, presence of additional tRNA genes and large non-coding regions as well as a CR duplication indicate intense rearrangement processes, which have occurred during the evolution of Baikalian amphipods. Such rearrangements are usually a result of two major mechanisms, i.e. duplication and subsequent loss of mitochondrial genome regions [112, 113] and intramitochondrial recombination [114]. It is likely that different number and type of rearrangements led to the observed patterns of gene order and variance in the non-coding regions in the mitochondrial genomes of Baikalian amphipods. To decipher the mechanisms behind the appearance of every pattern and to predict an ancestral pattern for the mitogenomes of Baikalian amphipods a further careful investigation with a more comprehensive dataset is necessary.

Phylogenetic inference

For morphological identification of Baikalian amphipod species in our study we used the most modern taxonomy [17]. This taxonomy become a result of successive revision of previous ones [13, 2022, 24, 26, 27]. Since new families were introduced in the course of recent revisions of Baikalian amphipods, some species and genera were renamed and thus the species list differs from the one given in the previous publications [28, 30, 35, 36]. To make the phylogenetic results of our work comparable with previous studies we considered them in the context of contemporary taxonomic system that combined all taxonomy alterations [17].

The phylogenetic analyses of amphipod species based on 13 concatenated mitochondrial protein coding gene sequences using Bayesian Inference (BI) resulted in a well-supported tree. The Baikalian species in the BI tree form a monophyletic group and the amphi-Atlantic amphipod species G. duebeni is the nearest outgroup to the Baikalian clade (Fig. 3).
Fig. 3
Fig. 3

Phylogenetic inference (BI) of amphipods based on 13 mitochondrial protein-coding genes sequences. Numbers above the branches indicate Bayesian posterior probabilities. Coloured rectangles denote depths of habitats of Baikalian amphipods. Yellow rectangles denote littoral species, green ones denote sub-littoral species, blue ones denote abyssal species

The previous phylogenetic inferences based on the cox3 gene fragment [36], 18S rRNA and the cox1 gene fragments [2835] as well as on a combined set of molecular data (rrnL and 18S rRNA, cox1 genes fragments) and morphological characters [30] and the most recent study, which involved four molecular markers (cox1, EF-1α, 18S and 28S rRNA) [32], revealed that different species of a genus Gammarus were included into a clade of Micruropodidae family. The phylogenetic trees derived in those studies had low support in many nodes. Utilization of 13 protein coding genes of the mitochondrial genome helped us to obtain a better supported tree of Baikalian amphipods in comparison with the ones described in previous molecular studies. The relatively small number of taxa sampled in our study does not allow us to rule out the possibility that the Baikalian clade might still be split into two or more independent lineages if more species are added to the analysis, particularly if G. lacustris is included. However, presently our data suggest that the common outgroup to all Baikalian species is the nearest sister species G. duebeni. This result corroborates the recent study by Hou and Sket (2016) [32].

The phylogenetic tree demonstrates separation of Baikalian amphipod species into two clades where the one includes species from the Micruropodidae and Crypturopodidae families and the other includes species from the Acanthogammaridae, Pallaseidae, and Eulimnogammaridae families (Fig. 3). This clusterization is in concordance with the current view on the existence of two major amphipod lineages in Lake Baikal, which is based on morphological investigations [25] and molecular phylogenetic data [3032, 35].

The phylogenetic tree obtained in our study can be used to make some assumptions about the origination of certain ecological features of Baikalian amphipods. The Baikalian amphipods C. tuberculatus, L. vortex and G. fasciatus, which comprise one of the lineages in our study (Fig. 3), are mainly shallow-water inhabitants, having smooth body and display tolerance to warm water [13, 14, 115, 116]. Ancestors of these species may have originated during the Tertiary period when the climate was warm [117] and therefore they may be warm-water relicts [14, 25]. The second lineage of Baikalian amphipods contains species that possess more diverse morphological features, lifestyle and ecological niches. The radiation of this lineage presumably coincided with the completion of climate cooling period in the late Eocene – early Oligocene according to Kamaltynov [14]. This lineage is subdivided into two clades: the first one includes armored and relatively shallow water species P. kesslerii (Pallaseidae) and A. victorii (Acanthogammaridae) [13, 14], the second clade consists of two armored deep-water predator species (G. cabanisii and B. grewingkii) and a derived clade of smooth littoral amphipods of Gen. Eulimnogammarus Bazikalova, 1945, which differ from the rest by their feeding habits. The separation of species from the second lineage into two clades is also supported by morphological features, as A.victorii and P.kesslerii possess more plesiomorphic traits in comparison to the rest of the species [13, 14]. The topology of the BI tree shows that the species of Eulimnogammarus genus may have originated from an ancestor inhabiting the abyssal zone of Lake Baikal. However, it is possible that an expanded sampling of Baikalian species may yet show the different trends of origination of the extant amphipods inhabiting different depths of the lake.

The topology of the BI tree revealed the paraphyly of family Acanthogammaridae, which in our study includes A.victorii, B.grewingkii and G.cabanisii. The phylogenetic separation of species within the Acanthogammaridae family (according to the contemporary taxonomy) was also observed in previous studies, though the trees in those studies were poorly resolved [28, 30, 35]. The Acanthogammaridae includes species with diverse morphological and ecological features united on the basis of armament characteristics [14]. However, according to Kamaltynov, the taxonomy of contemporary Acanthogammaridae still needs refinement. Some genera have features that may be sufficient for establishing new families. Additional molecular phylogenetic data including some nuclear markers and larger sampling of species from the Acanthogammaridae is necessary for the description of new families.

Conclusion

The detailed comparative study of mitochondrial genomes of endemic Baikalian amphipods belonging to the most diverse species flock of Lake Baikal is reported. The newly sequenced complete and nearly complete mitochondrial genomes of seven Baikalian species were presented in this study i.e. Acanthogammarus victorii, Crypturopus tuberculatus, Eulimnogammarus cyaneus, Garjajewia cabanisii, Gmelinoides fasciatus, Linevichella vortex and Pallaseopsis kesslerii.

The examined mitochondrial genome sequences were used to resolve phylogenetic relationships within the group of Baikalian amphipods. The branching order of the phylogenetic tree supports the separation of Baikalian species into two major lineages. Our data also support the paraphyly of Acanthogammaridae. The measurement of nucleotide diversity of protein-coding parts of Baikalian and non-Baikalian species allowed us to define the fragments of mitogenome most suitable for different scales of phylogenetic and/or population studies of amphipods.

The structural analysis of available Baikalian amphipod mitochondrial genomes revealed high variability in their length and gene order. Gene order of all mitochondrial genomes studied is changed relative to the pancrustacean ground pattern. Four species (G.cabanisii, E.vittatus, A.victorii and G.fasciatus) have extra tRNA genes copies. More severe rearrangements of protein coding genes and ribosomal RNA genes are found in P. kesslerii, C. tuberculatus and G. fasciatus. Multiple and unusually long intergenic spacers are found in mitochondrial genomes of B.grewingkii, P.kesslerii and G.fasciatus. Unusually high structural diversity of the amphipod mitochondrial genomes in Lake Baikal points at the possibility of high mutagenic pressure. This turns Baikalian amphipods into a potentially attractive model for studies of mitochondrial genome evolution in general.

Methods

Sampling, DNA extraction, mitochondrial genome amplification, sequencing

Amphipods species used for this study were collected in Lake Baikal from 2011 to 2013. Sampling was performed both manually at the water edge and by trawling from the ship at greater depths (Table 1). The species investigated in the current study were selected to maximally cover the range of species morphologies and ecological niches such as depth inhabited. Additional requirement was the ease of species diagnosis of the specimens.

Total DNA was extracted using modified CTAB method [118]. Depending on size of species we used either a whole animal or its part (a leg) for DNA extraction. The species identification was carried out using taxonomic system of Kamaltynov [17].

Total DNA samples of three out of seven amphipod species (G. fasciatus, A. victorii and G. cabanisii) was used directly for Illumina next generation sequencing libraries preparation. Paired-end libraries with insert size of 300 b.p. and 600 b.p. were prepared according to protocols provided by manufacturer for HiSeq (TruSeq DNA Sample Prep Kit) and MiSeq (Nextera DNA Library Preparation Kit) Systems (Illumina, San Diego, CA, USA).

Alternatively, DNA samples of other four species (P. kesslerii, L. vortex, C. tuberculatus and E. cyaneus) were used for long-range amplification of mitochondrial DNA. Mitochondrial genomes sequences were amplified as two fragments overlapping between cox1 to rrnL genes (Additional file 9). Primers were designed based on the alignment of cox1 and rrnL gene sequences of Baikalian amphipods available in GenBank. Additionally the universal Folmer’s primers were used [119]. The sequences of primers used in this study are available in Additional file 5.

Primers COI_L1 and 16S_H were used to amplify the c.a. 11Kb long (in all species) fragment spanning from cox1 to rrnL. PCR was performed using EncycloPlus PCR kit (Eurogen, Moscow, Russia). Each reaction contained 1 μl of 10× Encyclo buffer, 0.2 μl of dNTP Mixture (10 mM each), 0.5 μl of each primer, 1 μl of template DNA (10–50 ng), 0.2 μl of Encyclo polymerase mix and 6.6 μl of sterile water up to 10 μl. Amplification was carried out under following conditions: 95 °C for 1 min., followed by 30 cycles of 93 °C for 15 s., 60 °C for 15 s., 72 °C for 9 min., with final elongation at 72 °C for 3 min. Different pairs of primers were used to amplify the second fragment spanning from rrnL to cox1 in cases of different species as summarized in Additional file 5. PCR conditions were the same but the elongation times were decreased.

PCR products were purified by ethanol precipitation and were further utilized for libraries preparation using the Nextera DNA Library Preparation Kit (Illumina, San Diego, CA, USA) provided by manufacturer. The paired-end libraries with insert length of 600 b.p. were constructed and sequenced using MiSeq System (Illumina, San Diego, CA, USA).

Reads processing, mitochondrial genomes assembly and annotation

All sets of reads were cleaned from adapters, and parts with a quality score below 15 were trimmed using Trimmomatic-0.32 [120]. De-novo assembly was carried out with SPAdes 3.0.0 assembler [121]. Scaffolds of mitochondrial genome in the assemblies were identified using BLAST [122] and the reference sequences of amphipod E. verrucosus. Complete and nearly complete amphipod mitochondrial genome sequences obtained after assemblies were further used as reference sequences for mapping reads of appropriate species using Bowtie2 2.1.0 [123]. All generated read alignment files were used for manual correction of errors in reference sequences and for estimation of coverage depth. Visualization of read alignment files was made by Tablet 1.13.07.31 [124].

An automatic annotation of mitochondrial genome sequences was performed using the MITOS pipeline with default settings [125]. GenomeView browser [126] was used for visualization of annotation files and manual correction of gene boundaries. PCGs boundaries were verified by comparison with the orthologs of other amphipods and also taking into account adjacent tRNA genes positions [61]. rRNA genes boundaries were identified by comparison to mitochondrial rRNA genes sequences of other amphipods. tRNA genes and their secondary structures were predicted by MiTfi [127] as part of the MITOS pipeline [125].

Protein-coding genes analyses

Nucleotide composition and codon usage were calculated by The Sequence Manipulation Suite [128]. Effective number of codons was assessed using INCA 2.1 [129]. AT and GC skew of entire mitochondrial sequences were calculated using the following formulae: AT-skew = (A-T)/(A + T) and GC-skew = (G-C)/(G + C) [130]. Visualization of AT-skew and GC-skew plots as well as AT content plot for (+) strand were made by a custom Python script with a sliding window of 100 b.p. with steps of 10 b.p. Nucleotide diversity (Pi) was estimated for every protein-coding gene of Baikalian and non-Baikalian amphipods (see the list of species in Additional file 5) using DNAsp v.5 [131].

Phylogenetic inference

Protein coding nucleotide sequences were used for the phylogenetic inferences. Non-Baikalian amphipods were represented in the dataset by a single sequence for each species available in GeneBank by March 2016 (Additional file 5).

Each protein coding gene sequence set was aligned separately in codon-based fashion with TranslatorX web server [132] using ClustalW algorithm and then the sets were concatenated using Seaview 4.5.4 [133]. A resultant alignment contained 11,013 characters.

The best model of nucleotide substitution (GTR + I + G) was chosen with jModelTest [134]. The phylogenetic trees were built by MrBayes v. 3.2.1. [135]. Four independent runs of four MCMC chains were performed. Chains were run for five million generations, the first 30% of generations were discarded as burn-in. The resultant phylogenetic tree was visualized in FigTree v.1.4.2. [136]. Metacrangonictidae clade was used as a root of the tree.

Abbreviations

BI: 

Bayesian inference

CR: 

Control region

ENC: 

Effective number of codons

PCGs: 

Protein-coding genes

Declarations

Acknowledgments

Computational experiments have been performed with HPC cluster “Academician V.M. Matrosov” (Irkutsk Supercomputer Centre of SB RAS, http://hpc.icc.ru). We are grateful to the three anonymous reviewers for their valuable comments and suggestion that helped us to improve the manuscript.

Declarations

This article has been published as part of BMC Genetics Vol 17 Suppl 14, 2016: Selected articles from BGRS\SB-2016: genomics. The full contents of the supplement are available online at http://bmcgenomics.biomedcentral.com/articles/supplements/volume-17-supplement-14.

Funding

The work was supported by the governmentally funded project No 0345-2014-0005; Russian Foundation for Basic Research (Grants no. 15-04-05841, 15-07-03827 and 15-04-03848). Phylogenetic analysis in this study was supported by the Russian Science Foundation (Grant Number: 14-50-00029). The publication cost of this article has been funded by the Russian Foundation for Basic Research.

Availability of data and materials

All data generated or analysed during this study are included in this published article and its supplementary information files.

Authors’ contributions

EVR and DYS are responsible for conception and design of the study. EVR, DYS and EAS carried out taxonomic sampling. RMK performed the morphological identification of species. EVR performed the laboratory works. MDL performed the library preparation for Illumina Sequencing. KVM and EVR are responsible for assembly and annotation of mitochondrial genomes. DYS, VVA, RMK, EAS, AVG and ASA participated in statistical and phylogenetic analyses. EVR wrote the manuscript. All authors read and approved the final version of the manuscript.

Competing interests

The authors declared that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Not applicable.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.

Authors’ Affiliations

(1)
Laboratory of Molecular Systematics, Limnological Institute, Siberian Branch of Russian Academy of Sciences, Irkutsk, 664033, Russian Federation
(2)
Belozersky Institute for Physicochemical Biology, Lomonosov Moscow State University, Moscow, 119991, Russian Federation
(3)
Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow, 127994, Russian Federation
(4)
Extreme Biology Laboratory, Institute of Fundamental Medicine and Biology, Kazan Federal University, Kazan, 420012, Russian Federation
(5)
Institute for System Dynamics and Control Theory, Siberian Branch of Russian Academy of Sciences, Irkutsk, 664033, Russian Federation
(6)
Faculty of Biology and Soil Studies, Irkutsk State University, Irkutsk, 664003, Russian Federation

References

  1. Cristescu ME, Adamowicz SJ, Vaillant JJ, Haffner DG. Ancient lakes revisited: from the ecology to the genetics of speciation. Mol Ecol. 2010;19(22):4837–51.PubMedView ArticleGoogle Scholar
  2. Martens K. Speciation in ancient lakes. Trends Ecol Evol. 1997;12:177–82.PubMedView ArticleGoogle Scholar
  3. Schön I, Martens K. Adaptive, pre-adaptive and non-adaptive components of radiations in ancient lakes: a review. Org Divers Evol. 2004;4(3):137–56.View ArticleGoogle Scholar
  4. Kozhov MM. Biology of Lake Baikal. Moscow: AN SSSR Publication; 1963.View ArticleGoogle Scholar
  5. Kozhova OM, Izmest’eva LR, Baikal L. Evolution and Biodiversity. Leiden: Backhuys; 1998.Google Scholar
  6. Mats VD, Khlystov OM, De Batist M, Ceramicola S, Lomonosova TK, Klimansky A. Evolution of the Academician Ridge Accommodation Zone in the central part of the Baikal Rift, from high-resolution reflection seismic profiling and geological field investigations. Int J Earth Sci. 2000;89(2):229–50.View ArticleGoogle Scholar
  7. Brooks JL. Speciation in ancient lakes. Quart Rev Biol. 1950;25(1):30–60.View ArticleGoogle Scholar
  8. Mats VD. The structure and development of the Baikal rift depression. Earth Sci Rev. 1993;34(2):81–118.View ArticleGoogle Scholar
  9. Väinölä R, Kamaltynov RM. Species diversity and speciation in the endemic amphipods of Lake Baikal: molecular evidence. Crustaceana. 1999;72(8):945–56.View ArticleGoogle Scholar
  10. Mashiko K, Kamaltynov R, Morino H, Sherbakov DY. Genetic differentiation among gammarid (Eulimnogammarus cyaneus) populations in Lake Baikal, East Siberia. Arch Hydrobiol. 2000;148(2):249–61.View ArticleGoogle Scholar
  11. Daneliya ME, Kamaltynov RM, Väinölä R. Phylogeography and systematics of Acanthogammarus s.str., giant amphipod crustaceans from Lake Baikal. Zool Scr. 2011;40(6):623–37.View ArticleGoogle Scholar
  12. Bedulina DS, Takhteev VV, Pogrebnyak SG, Govorukhina EB, Madyarova EV, Lubyaga YA, et al. On Eulimnogammarus messerschmidtii, sp. n. (Amphipoda: Gammaridea) from Lake Baikal, Siberia, with redescription of E. cyanoides (Sowinsky) and remarks on taxonomy of the genus Eulimnogammarus. Zootaxa. 2014;3838(5):518–44.PubMedView ArticleGoogle Scholar
  13. Bazikalova AY. Lake Baikal amphipods. Proceedings of the Baikal Limnological Station. Moscow: Acad.Sci.Publishing House; 1945. p. 1–440.Google Scholar
  14. Kamaltynov RM. Amphipoda: Gammaroidea. In: Timoshkin OA, editor. Index of animal species inhabiting Lake Baikal and its catchment area. In 2 volumes. Vol. 1. Novosibirsk: Nauka; 2001. p. 572–832.Google Scholar
  15. Bazikalova AY. Bottom-living fauna. In: Galaziy GI, editor. Proceedings of Limnological Institute. Leningrad: Publishing House Nauka; 1971. p. 95–114.Google Scholar
  16. Takhteev VV, Mekhanikova IV. New species of the sideswimmers (Crustacea, Amphipoda) from the mountain streams of Khamar-Daban ridge. Researches of the water ecosystems of East Siberia Biodiversity of the Baikal Region. Irkutsk: Proceedings of the Biology and Soil Department of the Irkutsk State University Press; 2000.Google Scholar
  17. Kamaltynov RM. Amfipoda: Gammaroidea in Angara and Yenisei rivers. In: Timoshkin OA, Proviz VI, Sitnikova TY, Slugina ZV, Melnik NG, editors. Index of animal species inhabiting Lake Baikal and its catchment area. In 2 volumes. Vol. 2: Basins and channels in the south of East Siberia and North Mongolia. Novosibirsk: Nauka; 2009. p. 297–329.Google Scholar
  18. Mekhanikova IV, Chapelle G, De Broyer C. Echiuropus bekmanae n. sp. (Crustacea, Amphipoda, Carinagammaridae) from Lake Baikal, retrieved by a new deep-water sampling device. Hydrobiologia. 2001;462(1-2):241–51.Google Scholar
  19. Tachteev VV. Addition to revision of the genus Poekilogammarus (Crustacea, Amphipoda, Gammaridea) from Lake Baikal. Russian Journal of Zoology. 2000;79(6):649–61.Google Scholar
  20. Barnard JL, Barnard CM. Freshwater Amphipoda of the world. Vernon: Hayfield Associates; 1983.Google Scholar
  21. Bousfield EL. A new look at the systematics of gammaroidean amphipods of the world. Crustaceana. 1977;Suppl 4:282–316.Google Scholar
  22. Bousfield EL. Amphipoda. In: Parker SP, editor. Synopsis and classification of living organisms. New York: McGraw-Hill; 1982. p. 254–94.Google Scholar
  23. Daneliya ME, Kamaltynov RM, Kontula T, Väinölä R. Systematics of the Baikalian Babr (Crustacea: Amphipoda: Pallaseidae). Zootaxa. 2009;2276:49–68.Google Scholar
  24. Kamaltynov RM. On the present state of amphipod systematics. Hydrobiol J. 1993;26(6):82–92.Google Scholar
  25. Kamaltynov RM. On the evolution of Lake Baikal amphipods. Crustaceana. 1999;72(8):921–31.View ArticleGoogle Scholar
  26. Kamaltynov RM. On the higher classification of Lake Baikal amphipods. Crustaceana. 1999;72(8):933–44.View ArticleGoogle Scholar
  27. Takhteev VV. Essays on the amphipods of Lake Baikal (systematics, comparative ecology, evolution). Irkutsk: Irkutsk State University Press; 2000.Google Scholar
  28. Sherbakov DY, Kamaltynov RM, Ogarkov OB, Väinölä R, Vainio JK, Verheyen E. On the Phylogeny of Lake Baikal Amphipods in the Light of Mitochondrial and Nuclear Dna Sequence Data. Crustaceana. 1999;72(8):911–9.View ArticleGoogle Scholar
  29. Sherbakov DY. Molecular phylogenetic studies on the origin of biodiversity in Lake Baikal. Trends Ecol Evol. 1999;14(3):92–5.View ArticleGoogle Scholar
  30. MacDonald III KS, Yampolsky L, Duffy JE. Molecular and morphological evolution of the amphipod radiation of Lake Baikal. Mol Phylogenet Evol. 2005;35(2):323–43.PubMedView ArticleGoogle Scholar
  31. Hou Z, Sket B, Li S. Phylogenetic analyses of Gammaridae crustacean reveal different diversification patterns among sister lineages in the Tethyan region. Cladistics. 2014;30(4):352–65.View ArticleGoogle Scholar
  32. Hou Z, Sket B. A review of Gammaridae (Crustacea: Amphipoda): the family extent, its evolutionary history, and taxonomic redefinition of genera. Zool J Linn Soc. 2016;176(2):323–48.View ArticleGoogle Scholar
  33. Englisch U, Coleman CO, Wägele JW. First observations on the phylogeny of the families Gammaridae, Crangonyctidae, Melitidae, Niphargidae, Megaluropidae and Oedicerotidae (Amphipoda, Crustacea), using small subunit rDNA gene sequences. J Nat Hist. 2003;37(20):2461–86.View ArticleGoogle Scholar
  34. Väinölä R, Witt JDS, Grabowski M, Bradbury JH, Jazdzewski K, Sket B. Global diversity of amphipods (Amphipoda; Crustacea) in freshwater. Hydrobiologia. 2008;595(1):241–55.View ArticleGoogle Scholar
  35. Sherbakov DY, Kamaltynov RM, Ogarkov OB, Verheyen E. Patterns of evolutionary change in Baikalian gammarids inferred from DNA sequences (Crustacea, Amphipoda). Mol Phylogenet Evol. 1998;10(2):160–7.PubMedView ArticleGoogle Scholar
  36. Ogarkov OB, Kamaltynov RM, Belikov SI, Sherbakov DY. Phylogenetic relatedness of the Baikal Lake endemical [sic.] amphipods (Crustacea, Amphipoda) deduced from partial nucleotide sequences of the cytochrome oxidase subunit III genes. Mol Biol. 1997;31:24–9.Google Scholar
  37. Hou Z, Fu J, Li S. A molecular phylogeny of the genus Gammarus (Crustacea: Amphipoda) based on mitochondrial and nuclear gene sequences. Mol Phylogenet Evol. 2007;45(2):596–611.PubMedView ArticleGoogle Scholar
  38. Hou Z, Sket B, Fišer C, Li S. Eocene habitat shift from saline to freshwater promoted Tethyan amphipod diversification. Proc Natl Acad Sci U S A. 2011;108(35):14533–8.PubMedView ArticlePubMed CentralGoogle Scholar
  39. Bauza-Ribot MM, Jaume D, Juan C, Pons J. The complete mitochondrial genome of the subterranean crustacean Metacrangonyx longipes (Amphipoda): a unique gene order and extremely short control region. Mitochondrial DNA. 2009;20(4):88–99.PubMedView ArticleGoogle Scholar
  40. Bauza-Ribot MM, Juan C, Nardi F, Oromí P, Pons J, Jaume D. Mitogenomic phylogenetic analysis supports continental-scale vicariance in subterranean thalassoid crustaceans. Curr Biol. 2012;22(21):2069–74.PubMedView ArticleGoogle Scholar
  41. Ito A, Aoki MN, Yokobori S, Wada H. The complete mitochondrial genome of Caprella scaura (Crustacea, Amphipoda, Caprellidea), with emphasis on the unique gene order pattern and duplicated control region. Mitochondrial DNA. 2010;21(5):183–90.PubMedView ArticleGoogle Scholar
  42. Ki JS, Hop H, Kim SJ, Kim IC, Park HG, Lee JS. Complete mitochondrial genome sequence of the Arctic gammarid, Onisimus nanseni (Crustacea; Amphipoda): Novel gene structures and unusual control region features. Comp Biochem Physiol Part D Genomics Proteomics. 2010;5(2):105–15.PubMedView ArticleGoogle Scholar
  43. Kilpert F, Podsiadlowski L. The mitochondrial genome of the Japanese skeleton shrimp Caprella mutica (Amphipoda: Caprellidea) reveals a unique gene order and shared apomorphic translocations with Gammaridea. Mitochondrial DNA. 2010;21(3–4):77–86.PubMedView ArticleGoogle Scholar
  44. Krebes L, Bastrop R. The mitogenome of Gammarus duebeni (Crustacea Amphipoda): A new gene order and non-neutral sequence evolution of tandem repeats in the control region. Comp Biochem Physiol Part D: Genomics Proteomics. 2012;7(2):201–11.Google Scholar
  45. Pons J, Bauzà-Ribot MM, Jaume D, Juan C. Next- generation sequencing, phylogenetic signal and comparative mitogenomic analyses in Metacrangonyctidae (Amphipoda: Crustacea). BMC Genomics. 2014. doi:10.1186/1471-2164-15-566.Google Scholar
  46. Shin SC, Cho J, Lee JK, Ahn do H, Lee H, Park H. Complete mitochondrial genome of the Antarctic amphipod Gondogeneia antarctica (Crustacea, amphipod). Mitochondrial DNA. 2012;23(1):25–7.PubMedView ArticleGoogle Scholar
  47. Stokkan M, Jurado-Rivera JA, Juan C, Jaume D, Pons J. Mitochondrial genome rearrangements at low taxonomic levels: three distinct mitogenome gene orders in the genus Pseudoniphargus (Crustacea: Amphipoda). Mitochondrial DNA. 2016;27(5):3579–89.PubMedView ArticleGoogle Scholar
  48. Francino MP, Ochman H. Strand asymmetries in DNA evolution. Trends Genet. 1997;13:240–5.PubMedView ArticleGoogle Scholar
  49. Hassanin A, Leger N, Deutsch J. Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of Metazoa, and consequences for phylogenetic inferences. Syst Biol. 2005;54(2):277–98.PubMedView ArticleGoogle Scholar
  50. Kilpert F, Podsiadlowski L. The complete mitochondrial genome of the common sea slater, Ligia oceanica (Crustacea, Isopoda) bears a novel gene order and unusual control region features. BMC Genomics. 2006. doi:10.1186/1471-2164-7-241.
  51. Krapp T, Lang C, Libertini A, Melzer RR. Caprella scaura Templeton, 1836 sensu lato (Amphipoda: Caprellidae) in the Mediterranean. Org Divers Evol. 2006;6(2):77–81.View ArticleGoogle Scholar
  52. Boos K, Ashton GV, Cook EJ. The Japanese skeleton shrimp Caprella mutica (Crustacea, Amphipoda): a global invader of coastal waters. In: Galil BS, Clark PF, Carlton JT, editors. In the Wrong Place-Alien Marine Crustaceans: Distribution, Biology and Impacts. Netherlands: Springer; 2011. p. 129–56.View ArticleGoogle Scholar
  53. World Register of Marine Species. 2016. http://www.marinespecies.org at VLIZ. Accessed 10 Sept 2016.
  54. Jaumel D, Wagner HP. New cave-dwelling amphipods (Lysianassidae, Hadziidae) from the Dominican Republic (Hispaniola). Contrib Zool. 1998;68(1):37–66.Google Scholar
  55. Miloslavich P, Díaz JM, Klein E, Alvarado JJ, Díaz C, Gobin J, et al. Marine biodiversity in the Caribbean: regional estimates and distribution patterns. PLoS One. 2010. doi:10.1371/journal.pone.0011916.Google Scholar
  56. Gaston KJ, Spicer JI. The relationship between range size and niche breadth: a test of using five species of Gammarus (Amphipoda). Glob Ecol Biogeogr. 2001;10(2):179–88.View ArticleGoogle Scholar
  57. De Broyer C, Lowry JK, Jazdzewski K, Robert H. Catalogue of the Gammaridean and Corophiidean Amphipoda (Crustacea) of the Southern Ocean, with distribution and ecological data. In: De Broyer C, editor. Census of Antarctic Marine Life: Synopsis of the Amphipoda of the Southern Ocean. Vol. 1. Brussels: Edition of Royal Belgian Institute of Natural Sciences; 2007. p. 1–325.Google Scholar
  58. Wei SJ, Shi M, Chen XX, Sharkey MJ, van Achterberg C, Ye GY, et al. New views on strand asymmetry in insect mitochondrial genomes. PLoS One. 2010. doi:10.1371/journal.pone.0012708.Google Scholar
  59. Hassanin A. Phylogeny of Arthropoda inferred from mitochondrial sequences: Strategies for limiting the misleading effects of multiple changes in pattern and rates of substitution. Mol Phylogenet Evol. 2006;38(1):100–16.PubMedView ArticleGoogle Scholar
  60. Boore JL, Macey JR, Medina M. Sequencing and comparing whole mitochondrial genomes of animals. Meth Enzymol. 2005;395:311–48.PubMedView ArticleGoogle Scholar
  61. Ojala D, Montoya J, Attardi G. tRNA punctuation model of RNA processing in human mitochondria. Nature. 1981;290:470–4.PubMedView ArticleGoogle Scholar
  62. Wilson K, Cahill V, Ballment E, Benzie J. The complete sequence of the mitochondrial genome of the crustacean Penaeus monodon: are malacostracan crustaceans more closely related to insects than to branchiopods? Mol Biol Evol. 2000;17(6):863–74.PubMedView ArticleGoogle Scholar
  63. Wright F. The ‘effective number of codons’ used in a gene. Gene. 1990;87(1):23–9.PubMedView ArticleGoogle Scholar
  64. Lloyd RE, Foster PG, Guille M, Littlewood DT. Next generation sequencing and comparative analyses of Xenopus mitogenomes. BMC Genomics. 2012. doi:10.1186/1471-2164-13-496.PubMedPubMed CentralGoogle Scholar
  65. Mohandas N, Pozio E, La Rosa G, Korhonen PK, Young ND, Koehler AV, et al. Mitochondrial genomes of Trichinella species and genotypes – a basis for diagnosis, and systematic and epidemiological explorations. Int J Parasitol. 2014;44(14):1073–80.PubMedView ArticleGoogle Scholar
  66. Oliveira DC, Raychoudhury R, Lavrov DV, Werren JH. Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Mol Biol Evol. 2008;25(10):2167–80.PubMedView ArticlePubMed CentralGoogle Scholar
  67. Xiao JH, Jia JG, Murphy RW, Huang DW. Rapid evolution of the mitochondrial genome in Chalcidoid wasps (Hymenoptera: Chalcidoidea) driven by parasitic lifestyles. PLoS One. 2011. doi:10.1371/journal.pone.0026645.Google Scholar
  68. Zhao L, Zhang X, Tao X, Wang W, Li M. Preliminary analysis of the mitochondrial genome evolutionary pattern in primates. Dongwuxue Yanjiu. 2012;33(3–4):47–56.Google Scholar
  69. Xie Y, Niu L, Zhao B, Wang Q, Nong X, Chen L, et al. Complete mitochondrial genomes of chimpanzee- and gibbon-derived Ascaris isolated from a zoological garden in southwest China. PLoS One. 2013. doi:10.1371/journal.pone.0082795.Google Scholar
  70. Ye F, Liu T, King SD, You P. Mitochondrial genomes of two phlebotomine sand flies, Phlebotomus chinensis and Phlebotomus papatasi (Diptera: Nematocera), the first representatives from the family Psychodidae. Parasit Vectors. 2015. doi:10.1186/s13071-015-1081-1.Google Scholar
  71. Rivarola-Duarte L, Otto C, Juhling F, Schreiber S, Bedulina D, Jakob L, et al. A first glimpse at the genome of the Baikalian amphipod Eulimnogammarus verrucosus. J Exp Zool B Mol Dev Evol. 2014;322:177–89.PubMedView ArticleGoogle Scholar
  72. Lin FJ, Liu Y, Sha Z, Tsang LM, Chu KH, Chan TY, Liu R, Cui Z. Evolution and phylogeny of the mud shrimps (Crustacea: Decapoda) revealed from complete mitochondrial genomes. BMC Genomics. 2012. doi:10.1186/1471-2164-13-631.Google Scholar
  73. Liu Y, Cui Z. Complete mitochondrial genome of the Chinese spiny lobster Panulirus stimpsoni (Crustacea: Decapoda): genome characterization and phylogenetic considerations. Mol Biol Rep. 2011;38(1):403–10.PubMedView ArticleGoogle Scholar
  74. Shi H, Liu R, Sha Z, Ma J. Complete mitochondrial DNA sequence of Stenopus hispidus (Crustacea: Decapoda: Stenopodidea) and a novel tRNA gene cluster. Mar Genomics. 2012;6:7–15.PubMedView ArticleGoogle Scholar
  75. Masta SE. Mitochondrial sequence evolution in spiders: intraspecific variation in tRNAs lacking the TΨC arm. Mol Biol Evol. 2000;17(7):1091–100.PubMedView ArticleGoogle Scholar
  76. Campbell NJ, Barker SC. An unprecedented major rearrangement in an arthropod mitochondrial genome. Mol Biol Evol. 1998;15:1786–87.PubMedView ArticleGoogle Scholar
  77. Yamazaki N, Ueshima R, Terrett JA, Yokobori SI, Kaifu M, Segawa R, et al. Evolution of pulmonate gastropod mitochondrial genomes: comparisons of gene organizations of Euhadra, Cepaea and Albinaria and implications of unusual tRNA secondary structures. Genetics. 1997;145(3):749–58.PubMedPubMed CentralGoogle Scholar
  78. Okimoto R, Wolstenholme DR. A set of tRNAs that lack either the T psi C arm or the dihydrouridine arm: towards a minimal tRNA adaptor. EMBO J. 1990;9(10):3405–11.PubMedPubMed CentralGoogle Scholar
  79. Macey JR, Larson A, Ananjeva NB, Papenfuss TJ. Replication slippage may cause parallel evolution in the secondary structures of mitochondrial transfer RNAs. Mol Biol Evol. 1997;14(1):30–9.PubMedView ArticleGoogle Scholar
  80. Junqueira AC, Lessinger AC, Torres TT, da Silva FR, Vettore AL, Arruda P, et al. The mitochondrial genome of the blowfly Chrysomya chloropyga (Diptera: Calliphoridae). Gene. 2004;339:7–15.PubMedView ArticleGoogle Scholar
  81. Kocher A, Kamilari M, Lhuillier E, Coissac E, Péneau J, Chave J, Murienne J. Shotgun assembly of the assassin bug Brontostoma colossus mitochondrial genome (Heteroptera, Reduviidae). Gene. 2014;552(1):184–94.PubMedView ArticleGoogle Scholar
  82. Kim I, Lee EM, Seol KY, Yun EY, Lee YB, Hwang JS, Jin BR. The mitochondrial genome of the Korean hairstreak, Coreana raphaelis (Lepidoptera: Lycaenidae). Insect Mol Biol. 2006;15(2):217–25.PubMedView ArticleGoogle Scholar
  83. Sun S, Kong L, Yu H, Li Q. The complete mitochondrial DNA of Tegillarca granosa and comparative mitogenomic analyses of three Arcidae species. Gene. 2015;557(1):61–70.PubMedView ArticleGoogle Scholar
  84. Kumazawa Y, Nishida M. Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics. J Mol Evol. 1993;37(4):380–98.PubMedView ArticleGoogle Scholar
  85. Kakehashi R, Kurabayashi A, Oumi S, Katsuren S, Hoso M, Sumida M. Mitochondrial genomes of Japanese Babina frogs (Ranidae, Anura): unique gene arrangements and the phylogenetic position of genus Babina. Genes Genet Syst. 2013;88(1):59–67.PubMedView ArticleGoogle Scholar
  86. Liu C, Chang J, Ma C, Li L, Zhou S. Mitochondrial genomes of two Sinochlora species (Orthoptera): novel genome rearrangements and recognition sequence of replication origin. BMC Genomics. 2013. doi:10.1186/1471-2164-14-114.Google Scholar
  87. Cantatore P, Gadaleta MN, Roberti M, Saccone C, Wilson AC. Duplication and remoulding of tRNA genes during the evolutionary rearrangement of mitochondrial genomes. Nature. 1987;329:853–55.PubMedView ArticleGoogle Scholar
  88. Belinky F, Rot C, Ilan M, Huchon D. The complete mitochondrial genome of the demosponge Negombata magnifica (Poecilosclerida). Mol Phylogenet Evol. 2008;47(3):1238–43.PubMedView ArticleGoogle Scholar
  89. Lavrov DV, Lang BF. Transfer RNA gene recruitment in mitochondrial DNA. Trends Genet. 2005;21(3):129–33.PubMedView ArticleGoogle Scholar
  90. Wang X, Lavrov DV. Gene recruitment – a common mechanism in the evolution of transfer RNA gene families. Gene. 2011;475(1):22–9.PubMedView ArticleGoogle Scholar
  91. Sahyoun AH, Hölzer M, Jühling F, Höner zu Siederdissen C, Al-Arab M, Tout K, et al. Towards a comprehensive picture of alloacceptor tRNA remolding in metazoan mitochondrial genomes. Nucleic Acids Res. 2015;43(16):8044–56.PubMedView ArticlePubMed CentralGoogle Scholar
  92. Rawlings TA, Collins TM, Bieler R. Changing identities: tRNA duplication and remolding within animal mitochondrial genomes. Proc Natl Acad Sci U S A. 2003;100(26):15700–5.PubMedView ArticlePubMed CentralGoogle Scholar
  93. Rawlings TA, MacInnis MJ, Bieler R, Boore JL, Collins TM. Sessile snails, dynamic genomes: gene rearrangements within the mitochondrial genome of a family of caenogastropod molluscs. BMC Genomics. 2010. doi:10.1186/1471-2164-11-440.PubMedPubMed CentralGoogle Scholar
  94. Iannelli F, Griggio F, Pesole G, Gissi C. The mitochondrial genome of Phallusia mammillata and Phallusia fumigata (Tunicata, Ascidiacea): high genome plasticity at intra-genus level. BMC Evol Biol. 2007. doi:10.1186/1471-2148-7-155.PubMedPubMed CentralGoogle Scholar
  95. Kumazawa Y, Miura S, Yamada C, Hashiguchi Y. Gene rearrangements in gekkonid mitochondrial genomes with shuffling, loss, and reassignment of tRNA genes. BMC Genomics. 2014. doi:10.1186/1471-2164-15-930.PubMedPubMed CentralGoogle Scholar
  96. Macey JR, Larson A, Ananjeva NB, Fang Z, Papenfuss TJ. Two novel gene orders and the role of light-strand replication in rearrangement of the vertebrate mitochondrial genome. Mol Biol Evol. 1997;14(1):91–104.PubMedView ArticleGoogle Scholar
  97. Matsumoto Y, Yanase T, Tsuda T, Noda H. Species-specific mitochondrial gene rearrangements in biting midges and vector species identification. Med Vet Entomol. 2009;23(1):47–55.PubMedView ArticleGoogle Scholar
  98. Rawlings TA, Collins TM, Bieler R. A major mitochondrial gene rearrangement among closely related species. Mol Biol Evol. 2001;18(8):1604–9.PubMedView ArticleGoogle Scholar
  99. Saito S, Tamura K, Aotsuka T. Replication origin of mitochondrial DNA in insects. Genetics. 2005;171(4):1695–705.PubMedView ArticlePubMed CentralGoogle Scholar
  100. Cook CE. The complete mitochondrial genome of thestomatopod crustacean Squilla mantis. BMC Genomics. 2005. doi:10.1186/1471-2164-6-105.PubMedPubMed CentralGoogle Scholar
  101. Doublet V, Helleu Q, Raimond R, Souty-Grosset C, Marcade I. Inverted repeats and genome architecture conversions of terrestrial isopods mitochondrial DNA. J Mol Evol. 2013;77(3):107–18.PubMedView ArticleGoogle Scholar
  102. Shao R, Barker SC. The highly rearranged mitochondrial genome of the plague thrips, Thrips imaginis (Insecta: Thysanoptera): convergence of two novel gene boundaries and an extraordinary arrangement of rRNA Genes. Mol Biol Evol. 2003;20(3):362–70.PubMedView ArticleGoogle Scholar
  103. Zhang DX, Hewitt GM. Nuclear integrations: challenges for mitochondrial DNA markers. Trends Ecol Evol. 1996;11(6):247–51.PubMedView ArticleGoogle Scholar
  104. Romanova EV, Mikhailov KV, Logacheva MD, Kamaltynov RM, Aleoshin VV, Sherbakov DY. The complete mitochondrial genome of Baikalian amphipoda Eulimnogammarus vittatus Dybowsky, 1874. Mitochondrial DNA A DNA MappSeq Anal. 2016;27(3):1795–7.PubMedGoogle Scholar
  105. Romanova EV, Mikhailov KV, Logacheva MD, Kamaltynov RM, Aleoshin VV, Sherbakov DY. The complete mitochondrial genome of a deep-water Baikalian amphipoda Brachyuropus grewingkii (Dybowsky, 1874). Mitochondrial DNA. 2015. doi:10.3109/19401736.2014.1003891.PubMedGoogle Scholar
  106. Black 4th WC, Roehrdanz RL. Mitochondrial gene order is not conserved in arthropods: prostriate and metastriate tick mitochondrial genomes. Mol Biol Evol. 1998;15(12):1772–85.PubMedView ArticleGoogle Scholar
  107. Campbell NJ, Barker SC. The novel mitochondrial gene arrangement of the cattle tick, Boophilus microplus: fivefold tandem repetition of a coding region. Mol Biol Evol. 1999;16(6):732–40.PubMedView ArticleGoogle Scholar
  108. Ogoh K, Ohmiya Y. Complete mitochondrial DNA sequence of the sea-firefly, Vargula hilgendorfii (Crustacea, Ostracoda) with duplicate control regions. Gene. 2004;327(1):131–9.PubMedView ArticleGoogle Scholar
  109. Arndt A, Smith MJ. Mitochondrial gene rearrangement in the sea cucumber genus Cucumaria. Mol Biol Evol. 1998;15(8):1009–16.PubMedView ArticleGoogle Scholar
  110. Yang J, Ye F, Huang Y. Mitochondrial genomes of four katydids (Orthoptera: Phaneropteridae): New gene rearrangements and their phylogenetic implications. Gene. 2016;575(2):702–11.PubMedView ArticleGoogle Scholar
  111. Bernt M, Braband A, Schierwater B, Stadler PF. Genetic aspects of mitochondrial genome evolution. Mol Phylogenet Evol. 2013;69(2):328–38.PubMedView ArticleGoogle Scholar
  112. Boore JL. The duplication/random loss model for gene rearrangement exemplified by mitochondrial genomes of deuterostome animals. In: Sankoff D, Nadeau JH, editors. Comparative genomics. Dordrecht: Kluwer Academic Publishers; 2000. p. 133–47.View ArticleGoogle Scholar
  113. Lavrov DV, Boore JL, Brown WM. Complete mtDNA sequences of two millipedes suggest a new model for mitochondrial gene rearrangements: duplication and nonrandom loss. Mol Biol Evol. 2002;19(2):163–9.PubMedView ArticleGoogle Scholar
  114. Dowton M, Campbell NJH. Intramitochondrial recombination – is it why some mitochondrial genes sleep around? Trends Ecol Evol. 2001;16(6):269–71.PubMedView ArticleGoogle Scholar
  115. Bazikalova A. Systematics, ecology and distribution of genera Micruropus Stebbing and Pseudomicruropus nov. gen. (Amphipoda, Gammaridae). In: Galaziy GI, editor. System and ecology of Crustaceans of Lake Baikal. Moscow: Acad. Sci. Publishing House; 1962. p. 3–140.Google Scholar
  116. Bekman MYu. Ecology and production of Micruropus possolskii sow. and Gmelinoides fasciatus stebb. In: Galaziy GI, editor. System and ecology of crustaceans of Lake Baikal. Moscow: Acad. Sci. Publishing House; 1962. p. 141–56.Google Scholar
  117. Vorobiova GA, Matz VD, Shimaraeva MK. Late-Cenozoic paleoclimates in the Baikal region. Russian Journ Geol Geophys. 1995;36(8):82–96.Google Scholar
  118. Doyle JJ, Dickson E. Preservation of plant samples for DNA restriction endonuclease analysis. Taxon. 1987;36:715–22.View ArticleGoogle Scholar
  119. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3(5):294–9.PubMedGoogle Scholar
  120. Bolger AM, Lohse M, Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–20.PubMedView ArticlePubMed CentralGoogle Scholar
  121. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19(5):455–77.PubMedView ArticlePubMed CentralGoogle Scholar
  122. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–402.PubMedView ArticlePubMed CentralGoogle Scholar
  123. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–9.PubMedView ArticlePubMed CentralGoogle Scholar
  124. Milne I, Stephen G, Bayer M, Cock PJA, Pritchard L, Cardle L, et al. Using Tablet for visual exploration of second-generation sequencing data. Brief Bioinform. 2013;14(2):193–202.PubMedView ArticleGoogle Scholar
  125. Bernt M, Donath A, Juhling F, Externbrink F, Florentz C, Fritzsch G, Putz J, et al. MITOS: Improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol. 2013;69(2):313–9.PubMedView ArticleGoogle Scholar
  126. Abeel T, Van Parys T, Saeys Y, Galagan J, Van de Peer Y. GenomeView: a next-generation genome browser. Nucleic Acids Res. 2012. doi:10.1093/nar/gkr995.PubMedGoogle Scholar
  127. Juhling F, Putz J, Bernt M, Donath A, Middendorf M, Florentz C, et al. Improved systematic tRNA gene annotation allows new insights into the evolution of mitochondrial tRNA structures and into the mechanisms of mitochondrial genome rearrangements. Nucleic Acids Res. 2012;40(7):2833–45.PubMedView ArticleGoogle Scholar
  128. Stothard P. The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques. 2000;28(6):1102–4.PubMedGoogle Scholar
  129. Supek F, Vlahovicek K. INCA: synonymous codon usage analysis and clustering by means of self-organizing map. Bioinformatics. 2004;20(14):2329–30.PubMedView ArticleGoogle Scholar
  130. Perna NT, Kocher TD. Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol. 1995;41(3):353–8.PubMedView ArticleGoogle Scholar
  131. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003;19(18):2496–7.PubMedView ArticleGoogle Scholar
  132. Abascal F, Zardoya R, Telford MJ. TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res. 2010. doi:10.1093/nar/gkq291.PubMedPubMed CentralGoogle Scholar
  133. Gouy M, Guindon S, Gascuel O. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27(2):221–4.PubMedView ArticleGoogle Scholar
  134. Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol. 2008;25(7):1253–6.PubMedView ArticleGoogle Scholar
  135. Ronquist F, Huelsenbeck JP. Mrbayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–4.PubMedView ArticleGoogle Scholar
  136. Rambaut A. FigTree-v1.4.2. 2014. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 12 Oct 2014.

Copyright

© The Author(s). 2016

Advertisement