Mitogenomic sequences and evidence from unique gene rearrangements corroborate evolutionary relationships of myctophiformes (Neoteleostei)
© Poulsen et al.; licensee BioMed Central Ltd. 2013
Received: 17 February 2012
Accepted: 20 May 2013
Published: 3 June 2013
A skewed assemblage of two epi-, meso- and bathypelagic fish families makes up the order Myctophiformes – the blackchins Neoscopelidae and the lanternfishes Myctophidae. The six rare neoscopelids show few morphological specializations whereas the divergent myctophids have evolved into about 250 species, of which many show massive abundances and wide distributions. In fact, Myctophidae is by far the most abundant fish family in the world, with plausible estimates of more than half of the oceans combined fish biomass. Myctophids possess a unique communication system of species-specific photophore patterns and traditional intrafamilial classification has been established to reflect arrangements of photophores. Myctophids present the most diverse array of larval body forms found in fishes although this attribute has both corroborated and confounded phylogenetic hypotheses based on adult morphology. No molecular phylogeny is available for Myctophiformes, despite their importance within all ocean trophic cycles, open-ocean speciation and as an important part of neoteleost divergence. This study attempts to resolve major myctophiform phylogenies from both mitogenomic sequences and corroborating evidence in the form of unique mitochondrial gene order rearrangements.
Mitogenomic evidence from DNA sequences and unique gene orders are highly congruent concerning phylogenetic resolution on several myctophiform classification levels, corroborating evidence from osteology, larval ontogeny and photophore patterns, although the lack of larval morphological characters within the subfamily Lampanyctinae stands out. Neoscopelidae is resolved as the sister family to myctophids with Solivomer arenidens positioned as a sister taxon to the remaining neoscopelids. The enigmatic Notolychnus valdiviae is placed as a sister taxon to all other myctophids and exhibits an unusual second copy of the tRNA-Met gene – a gene order rearrangement reminiscent of that found in the tribe Diaphini although our analyses show it to be independently derived. Most tribes are resolved in accordance with adult morphology although Gonichthyini is found within a subclade of the tribe Myctophini consisting of ctenoid scaled species. Mitogenomic sequence data from this study recognize 10 reciprocally monophyletic lineages within Myctophidae, with five of these clades delimited from additional rearranged gene orders or intergenic non-coding sequences.
Mitogenomic results from DNA sequences and unique gene orders corroborate morphology in phylogeny reconstruction and provide a likely scenario for the phylogenetic history of Myctophiformes. The extent of gene order rearrangements found within the mitochondrial genomes of myctophids is unique for phylogenetic purposes.
Lanternfishes (Myctophidae) and blackchins (Neoscopelidae) comprise the only two families in the order Myctophiformes, superorder Scopelomorpha , a group currently including some 250 species . The 32 genera of Myctophidae contain about 98% of the species diversity, and morphological characters have clearly shown Myctophidae more derived compared to the more generalized Neoscopelidae [3–6]. Myctophids are exclusively marine and pelagic, occupying depths from surface waters down to the upper 1000 meters of the bathypelagic layer (1000–4000 meters). The group as a whole constitutes fairly small fishes ranging in size from 20 to 300 millimeters, with larger members being confined to the bathypelagic realm. They are ubiquitous in the World’s oceans and exhibit extremely high abundances with one estimate as high as 65% of all pelagic deep-sea fish biomass .
Diel vertical migration (DVM) is a prominent feature of myctophids although not all myctophid species engage in this activity . DVM prompted the famous “false bottom” (or the deep scattering layer) discovery, turning out to be massive occurrences of the swimbladder-possessing myctophid Ceratoscopelus maderensis among other deep-sea animals . DVM is common across many animal groups and is generally believed to involve feeding and/or reduced predation risk associated with reduced light intensity . Herring  notes that if populations are biased towards horizontal layers, as is often the case with myctophids, DVM might be an effective way to channel intra-specific encounters and could be important in mate recognition. A phylogenetic component in DVM has not been explored although DVM is clearly more pronounced in some groups of myctophids than others, e.g. the slendertails of the tribe Gonichthyini including the genera Gonichthys, Centrobranchus, Tarletonbeania and Loweina.
Surprisingly little molecular work has been carried out on Myctophiformes considering their abundance and at times problematic species identification. Yamaguchi et al.  tested photophore patterns, biogeographical distributions and diverse larval eye morphology within Hygophum in a phylogenetic context. The results indicated all three attributes as somewhat informative concerning speciation pattern, although clear conclusions were hard to extract due to few characters (partial 16S rRNA gene sequences) and incomplete taxon sampling. However, with an increasing understanding of myctophiform phylogeny, this type of study will become highly valuable in terms of assessing open-ocean speciation patterns in myctophids as well as other open-ocean fish components .
Miya et al.  produced the first mitochondrial (mt) genome mapping of myctophiform fishes, showing that the two myctophids Diaphus splendidus and Myctophum affine possess non-typical vertebrate mt gene arrangements, whereas the neoscopelid fish Neoscopelus microchir exhibits the typical gene arrangement for vertebrates . Their findings indicated that mt gene arrangements of myctophid fishes have the potential to provide evidence concerning clade delimitation at various levels. Clade-specific gene orders are considered strong evidence for monophyly since the process of gene duplication and subsequent deletions are considered random and rare events [35–39]. However, accumulating evidence shows positive selection on some rearranged mt gene orders  to be much more common than initially expected . Intergenic non-coding (INC) regions are likewise believed to provide evidence for phylogenetic history, although this group of markers has been poorly explored mainly because of insufficient taxon sampling.
This study is the first to use mitogenomic DNA sequences combined with additional information from extensively rearranged gene orders and INC-sequences to explore myctophiform phylogeny.
87 taxa included in this study
Voucher Museum #
Ishiguro et al. 2003 
Ishiguro et al. 2003 
Miya & Nishida 2000 
Yasuike et al. 2010
Doiron et al. 2002
Ishiguro et al. 2003 
Ishiguro et al. 2003 
Ishiguro et al. 2003 
Ishiguro et al. 2003 
Ishiguro et al. 2003 
Ishiguro et al. 2003 
Li et al. 2010
Ishiguro et al. 2001
Miya & Nishida 2000 
Miya et al. 2001 
Miya & Nishida 1999 
Miya et al. (unpubl.)
Ishiguro et al. 2003 
Li et al. 2010
Chen & Wu (unpubl.)
Miya et al. 2001 
Kawaguchi et al. 2001 
Miya et al. 2001 
Miya et al. 2001 
Miya et al. 2001 
Miya et al. 2001 
Miya et al. 2001 
Miya et al. 2001 
Miya et al. 2001 
Miya et al. 2001 
Miya et al. 2001 
Lampadena urophaos atlantica
Miya et al. 2001 
Miya et al. 2003 
Miya et al. 2003 
Miya et al. 2003 
Miya et al. 2010 
Miya et al. 2010 
Miya et al. 2010 
Miya et al. 2001 
Miya et al. 2003 
Miya & Nishida 2000 
Miya et al. 2001 
Miya et al. 2007
Miya et al. 2003 
Satoh et al. 2006 
Miya et al. 2003 
Miya et al. 2001 
Miya et al. 2003 
Miya et al. 2003 
Production of mitogenomic data
Genomic DNA was extracted using the Qiagen Puregene extraction kit following the manufacturer´s protocol and used directly for long and accurate amplification PCR (LA PCR) of the entire mitochondrial genome . Depending on tissue quality and LA primer fidelity, a variable number of LA PCR reactions were needed for complete coverage, with a minimum of two and a maximum of six for some species. The LA PCR product was diluted with ddH2O according to success of amplification and nested short PCR was subsequently performed on the LA product with a broad range of fish universal and species specific primers (>200). Double stranded PCR products were cleaned with Exo-Sap at 60°C for 60 minutes and used as template for direct cycle-sequencing with dye labeled terminators (Applied Biosystems). All fragments were sequenced on automated DNA sequencers according to length of labelled fragments. Quality of tissue was shown to be a prominent obstacle regarding successful amplifications. Issues regarding amplification necessitated multiple PCR protocols and tailor-made primer sets for different taxa. Variable number tandem repeats found in the control region and various INC-regions added to the technical issues. Primer information and protocols regarding PCR and sequencing for particular species are available by request (JYP). Newly determined mitogenome sequences are available as [DDBJ, EMBL or GenBank AP012227-62, AP0122264 and AB648909-10] (Table 1).
Sequence editing, alignment and analyses
Raw sequence data were processed and formatted with the software 4peaks Ver. 1.7.2 , Textwrangler Ver. 3.5.3  and MacClade Ver. 4.06  at various stages before alignment. Mitogenome assembly was performed using Sequencher Ver. 4.10.1  by concatenation of overlapping sequences. Numerous single nucleotide repeat regions were concatenated from the L- and H-strand sequences assuming the repeat region to be identical in the two strands. This was verified by electrophoresis of the sequenced PCR products showing bands with equal size to the sequenced fragments. All genes were initially annotated by alignment to those from closely related fishes already available in GenBank . Subsequently, protein coding genes were examined by reference to ORFs and the 22 tRNA genes were examined for secondary structure by tRNAscan-SE Ver. 1.21 [55, 56]. The two ribosomal RNA genes (12S and 16S) were annotated as the sequences between flanking tRNA Phe, Val and LeuUUR in addition to alignment using previously determined myctophid RNA genes .
Alignment of the 12 protein coding genes was done by eye whereas the 22 tRNA genes and 12S+16S rRNA genes were aligned with a probabilistic multiple alignment approach using ProAlign Ver. 0.5 . The ND6 gene was excluded due to heterogeneous base composition  leaving 10908 protein coding nucleotide characters (3636 amino acids). Ambiguous alignment of the tRNA and rRNA genes were discarded from the analyses based on the 90% minimum posterior probability of correct alignment implemented in ProAlign, leaving 938 and 1474 nucleotide characters from 22 tRNA and 12S+16S rRNA genes, respectively. All genes were aligned separately and subsequently concatened into one dataset consisting of six partitions as suggested by PartitionFinder  (see Additional file 1); amino acids, 12S+16S rRNA genes and 22 concatenated tRNA genes (designated as 123ARTn). Missing nucleotides, e.g. tRNA-Thr and Pro genes for some species, were coded as missing characters. Levels of mutational saturation were calculated from p-distances for 1st, 2nd and 3rd codon positions using PAUP* Ver. 4.0b10  (see Additional file 2). Since no mutational saturation was detected when including only myctophiforms, we constructed a second dataset consisting of only nucleotides from the 41 myctophiform species. This dataset included all mitogenomic nucleotides except the CR and ProAlign ambiguous alignment as already noted above (123nRTn).
Heuristic maximum likelihood phylogenetic analyses with 1000 non-parametric bootstrap replications for all nodes were performed in a single run with the sequential version of RAxML Ver. 7.2.8 [60, 61] under the GTR+Γ+I substitution model  as chosen by Akaike and Bayesian information criteria [63, 64] implemented in Modelgenerator . A final ML optimization of every 5th bootstrapped tree for the highest scoring ML-tree is performed by RAxML under the specified GTR+Γ+I substitution model . Partitions constructed from amino acids were analyzed with the mtREV model  chosen by Modelgenerator.
Bayesian analysis was performed on the datasets with MrBayes Ver. 3.2.1  using the same partitions and models as described above. Maximum likelihood analyses were conducted on a Quad-core Mac Pro desktop computer whereas the Bayesian analyses were computed on the Bioportal computer cluster University of Oslo . Convergence of chains and burn-in were determined using TRACER Ver. 1.5 .
Additional analyses and diaphini tRNA-met pseudogenes
All 41 myctophiform mitogenomes were scrutinized for mt features such as rearranged gene orders and INC-regions. All INC-sequences were analyzed for sequence similarity in relation to possible duplicated regions in the mitochondrial genome by using NCBI Blast , tRNAscan  and a series of decreasing assembly parameters in Sequencher . Subsequently, alignments of INC-regions were examined for secondary folding patterns with LocARNA Ver. 1.5.2  and RNAshapes Ver. 2.1.6  in order to detect conserved regions. Secondary tRNA-structures were drawn with VARNA Ver. 3.8 . In order to examine a putative associated gene order found in Notolychnus and species within the tribe Diaphini, neighbour-joining analyses were carried out including multiple myctophid tRNA-Met genes, putative duplicated diaphinid tRNA-Met genes (pseudogenes) and the two tRNA-Met genes observed in Notolychnus. Pairwise sequence variation of the pseudogenes and detected tRNA-Met genes in Diaphini were compared in order to validate the INC-regions as actual tRNA-Met pseudogenes, the latter expected to show higher substitution rates.
Testing alternative phylogenetic hypotheses
Topology comparison from morphological phylogenies and this study were tested by using the approximately unbiased log-likelihood test  implemented in CONSEL . Constrained trees were produced with Mesquite  and per-site log-likelihood scores were produced using RAxML using the f –g option with best scoring ML-trees passed via –z option. Per-site log-likelihood scores and tree topologies were used as direct input into CONSEL outputting tree-specific ML-scores and associated p-values.
WANYC-gene order found in all myctophids. The tRNA-Cys and Tyr have shifted positions and the putative OL-region was much longer than the usual vertebrate sequence in this region of about 30–40 base pairs (56–321 in myctophids included in this study). We were not able to find any conserved sequence blocks or secondary cloverleaf structure typical of tRNA genes  for this INC-region (see Additional file 3).
IMQMψ gene order found in the tribe Diaphini. The tRNA-Gln and Met have shifted positions with the typical L- and H-strand coding intact (tRNA-Gln is coded on the L-strand and tRNA-Met coded on the H-strand). An INC-region (tRNA-Met pseudogene denoted as Mψ) is present between tRNA-Gln and ND1 in all diaphinid taxa included. A similar gene order was also observed for Notolychnus valdiviae although the INC-region is a tRNA-Met gene for this taxon (IMQM gene order). This particular gene rearrangement was analyzed and is discussed in detail below.
Relocation of tRNA-Glu resulting in gene order Cytb/T/E/P in a Lampanyctini subclade. Species included within Lampanyctus, Nannobrachium, Stenobrachius and Triphoturus all show tRNA-Glu pseudogenes in the canonical position between ND6 and Cytb, verified from sequence comparisons and partial secondary cloverleaf structures (see Additional file 3). We were only able to determine the position of the tRNA-Glu gene in two of the five taxa, Nannobrachium ritteri and Lampanyctus crocodilus, all showing the novel position of tRNA-Glu between tRNA-Thr and Pro. A highly variable region downstream the CR and multiple nucleotide repeats prevented us from determining this sequence in Lampanyctus macdonaldi, Stenobrachius leucopsarus and Triphoturus nigrescens.
Cytb/T/ND6/E/P gene order in a Myctophini subclade. Myctophum punctatum, M. affine and M. nitidulum showed this rearranged gene order whereas M. asperum and M. orientale showed the canonical gene order. Unknown technical issues prevented us from determining the sequence of ND6 in M. punctatum although the gene rearrangement is evident also in this species from ND5/Cytb contiguous sequences as opposed to the canonical ND5/ND6/E/Cytb gene order.
INC-sequence between LeuUUR and ND1 found in all myctophids. This spacer ranged from 45–79 base pairs and showed no secondary structure or sequence similarity to any other mt genes (see Additional file 3).
INC-sequence between ND1 and tRNA-Ile found in Electronini. This spacer showed significant length variation and we were unable to determine the whole sequence in Protomyctophum arcticum.
INC-sequence between ATP6 and CO3 found in all myctophids. This spacer was 288 base pairs long in Notolychnus valdiviae and ranged from 9–43 base pairs in all other myctophids. We found no mt gene similarity or secondary structure for this INC-region (see Additional file 3).
INC-sequence associated with tRNA-Gly found in a Myctophini subclade. This INC-region is treated as a character state for the clade comprising Benthosema and Diogenichthys although the exact position varies between the two genera. The three species of Benthosema included showed the INC-region located upstream the tRNA-Gly whereas in Diogenichthys atlanticus, the spacer was located downstream tRNA-Gly. Electrona antarctica showed a different organization with two detected tRNA-Gly genes separated by a large INC-region. We found no sequence similarity to other mt genes for this region or any secondary folding structures (see Additional file 3).
Additional gene orders and INC-sequences were observed for various myctophid species although none of the rearrangements were distributed across multiple taxa at this point. These additional gene order rearrangements and INC-sequences are also presented in Figure 3. Detailed information for rearranged gene orders such as length of INC-sequences and missing regions is presented in the supplementary material (see Additional file 4). The highly polymorphic control region (CR) was consistently problematic to amplify or sequence, resulting in parts of the CR missing for most species as well as flanking tRNA-Thr and -Pro for some species.
Neoscopelidae and Myctophidae were both recovered as monophyletic with Scopenlengys tristis recovered as the sister taxon to the remaining neoscopelids (low support) and Notolychnus valdiviae was recovered as the sister taxon to the remaining myctophids (high support). Myctophine and lampanyctine subfamilies were also recovered as monophyletic in all analyses. The tribe Diaphini was recovered as the sister lineage to the other lampanyctines, found in all analyses although with low support values, despite the unresolved tribal relationships within the remaining lampanyctines. The tribe Electronini was recovered as the sister lineage to the other myctophines with maximum levels of support and a clade consisting of Benthosema spp. and Diogenichthys atlanticus was resolved as the sister lineage to the tribes Gonichthyini and Myctophini. Ten myctophid lineages are recognized from this study and are noted according to current tribal classification as A-J in Figures 4 and 5. We note that deep myctophiform- and tribe-defining nodes were consistently found in all analyses, although support values indicate uncertainty concerning basal neoscopelid-, basal lampanyctine- and to a lesser degree basal myctophine phylogenetic relationships. Tribal relationships within Lampanyctinae (clades D, E and F) proved to be the most problematic part of myctophid phylogenetics from mitogenomics, showing incongruent results between datasets employed and mode of analysis (Figures 4 and 5).
Diaphini tRNA-Met pseudogenes
Testing alternative phylogenetic hypotheses
Statistical comparisons between phylogenetic hypotheses using the AU-test (41 taxa Myctophiformes dataset)
Δ ln L
(Notolychnus (Lampanyctinae, Myctophinae))
((Notolychnus, Lampanyctinae) Myctophinae))
(Notolychnus, Myctophinae) Lampanyctinae)
(((Notolychnus, Diaphini) Lampanyctinae) Myctophinae)
Monophyly of myctophiformes and the two families
This study recovered a monophyletic Myctophiformes and monophyletic families with Neoscopelidae as the sister family of the highly diversified Myctophidae (Figures 4 and 5; [3, 5, 81, 82] although see Rosen ). We found Scopelengys tristis was a sister taxon to the remaining neoscopelids, including the monotypic endemic Sulu Sea taxon Solivomer arenidens, in congruence with morphology (Figure 2). Stiassny  presented characters in support for Scopelengys as sister taxa to the remaining neoscopelids, although she did note a possibility of apparently derived characters in Neoscopelus and Solivomer being secondarily reduced in Scopelengys. Analyses from the present study are congruent on this matter although support values are alarmingly low concerning the phylogenetic position of Solivomer arenidens. We found Notolychnus valdiviae to be the sister taxon to the remaining myctophids; however, morphological character states of Notolychnus such as dorsally located photophores, small larvae without pigmentation and a reduced otolith, have been extremely difficult to interpret concerning early myctophid divergence. Photophores are present in all myctophids except Taaningichthys paurolychnus and present only in one Neoscopelidae genus Neoscopelus. Our results show both of these genera nested within their respective families and the evolution of photophores within Myctophiformes is difficult to assess, i.e. whether photophores have evolved once or twice within ancestral myctophiforms. This question is pertinent from morphological considerations on photophore structure in Myctophidae and Neoscopelidae, as it is quite different in the two groups [85, 86]. The phylogenetic positions of Scopelengys/Solivomer and Notolychnus in this study revives an interesting observation by Paxton  concerning parallel evolutionary trends for Solivomer/Lampanyctinae and for Neoscopelus/Myctophinae, regarding changes in jaw length and characters possibly associated with these changes. These characters have been difficult to interpret in terms of polarity and this study supports long jaw length as the plesiomorphic state in Neoscopelidae and Myctophidae from the basal branchings of Scopelengys/Solivomer and Notolychnus. Also, Stiassny  noted that important myctophiform character states like elongated jaw length and raised photophores show ambiguity concerning early myctophiform divergence.
A monophyletic Myctophidae was strongly supported by mitogenome sequences, a WANYC gene order and an INC-spacer between tRNA-LeuUUR and ND1 (Figures 3 and 4). Rearrangement of the canonical vertebrate WANCY gene order was shared by all myctophids with the tRNA-Cys relocated downstream resulting in a synapomorphic WANYC gene order (Figure 5). A prolonged sequence (putative OL + INC-sequence) in the canonical position of the putative origin of L-strand replication was found within all myctophids (see Additional file 4), although fishes within the tribe Electronini were difficult to determine due to additionally rearranged gene orders in this region (Figure 3). An INC-region between the tRNA-LeuUUR and ND1 also represents synapomorphic evidence for Myctophidae (Figure 3). The size of this spacer ranged from 45–79 base pairs and we found no obvious tendency regarding size change for this INC-region (see Additional file 4). Neither the OL + INC-region nor the LeuUUR/ND1 spacers showed sequence similarity in any species to any other mitochondrial genes. Neither could they be folded into clover shape secondary structures, so their origins are elusive. On the other hand, assembly of the INC-spacers showed clear sequence similarity within genera indicating the INC-regions to be inherited synapomorphic characters within the family. Smith et al.  reported a length expansion for a similar small INC-sequence located between tRNA-Val and 12S rRNA in a clade of serranid fairy basslet fishes (Serranidae). They showed the INC-sequence to be homologous for all genera from simultaneous analysis of nucleotides and gene order – a very difficult task for myctophids considering multiple gene order rearrangements and putative associated INC-sequences. The third myctophid synapomorphy from this study is an INC-region between ATP6 and CO3 ranging from 288 base pairs in Notolychnus to 9–43 base pairs in the remaining myctophids included (see Additional file 4). No conserved sequence motifs were found in this region. This is a peculiar spacer in the sense that the canonical vertebrate gene order for this region is ATP6/CO3 with no tRNA gene acting as punctuation mark for RNA processing.
Monophyly of the two subfamilies and five tribes
The monophyly of the two subfamilies Lampanyctinae and Myctophinae was recovered from all analyses, although the low support values associated with this split are incomprehensible from morphological characters unambigously delimiting these two groups. As with the Myctophidae, the two subfamilies are fully supported by adult and larval morphology and no discussion is needed – character states are presented by Moser & Ahlstrom , Paxton  and Stiassny . A well supported result from this study, differing from morphology, is the phylogenetic position of the tribe Diaphini within Lampanyctinae, resolved as sister tribe to the other lampanyctines. Adult and larval morphology within Lampanyctinae show incongruences and both hypotheses are different compared to our molecular results (Figures 2, 4 and 5).This shows problematic morphological characters, lampanyctine larval characters are noted as few and tentative in previous larval studies [30, 88] and of little use above genus level, as well as molecular characters, no unique gene orders connect tribes and the mitogenomic phylogenetic sequence information is insufficient, as witnessed from the three different resolved Lampanyctinae topologies from this study (Figures 4 and 5).
Monophyly of the tribes Notolychnini (clade A in Figures 4 and 5), Diaphini (B), Gymnoscopelini (C), Lampanyctini (D+E+F), Electronini (G) and two subclades of Myctophini (H and I+J) are strongly supported from all mitogenomic DNA sequence analyses and various mt gene orders discussed below. Only the node delimiting the tribe Diaphini (B) show relatively low support values. The tribe Gonichthyini is tentatively placed from a single taxon as nested within a Myctophini subclade consisting of ctenoid-scaled species. Mitogenomic DNA sequence data from this study supports recognition of 10 mutually exclusive clades within Myctophidae (Figures 4 and 5).
Phylogeny of tribes and genera
Students of lanternfish phylogenetics will note the position of Notolychnus (clade A) resolved as sister taxon to the remaining family Myctophidae from mitogenome sequences. Paxton  tentatively placed Notolychnus as sister taxon to the subfamily Lampanyctinae (Figure 2A). Subsequent parsimony analysis of the same data by Paxton et al. , including additional larval characters [27–29], placed Notolychnus in an unresolved Myctophinae-Notolychnini-Lampanyctinae trifurcation (Figure 2D). Subsequently, Stiassny  added four additional characters and reanalyzed the aforementioned data with a similar result, showing Notolychnus as the sister taxon to the remaining lampanyctines (Figure 2E). Most recently, Yamaguchi  scrutinized previously published characters (Figure 2A-E) once again and reanalyzed the data, resulting in a largely unresolved myctophid tree (Figure 2F). However, the position of Notolychnus was congruent with Paxton  and Stiassny . The novel phylogenetic position of Notolychnus from this study, as the basal branching in Myctophidae, highlight the past issues concerning subfamilial affiliation and partly explains the lack of phylogenetically informative morphological characters in relation to the two subfamilies.
A monophyletic Diaphini (clade B) was well supported from both sequences and a unique IMQ-gene order (Figure 3), all in complete agreement with morphology, showing Lobianchia (2 species) as sister group of the very speciose Diaphus (78 species) [89–91]. Four species-groups of Diaphus have been suggested from the presence of Dn-Vn, Ant, Suo and So photophores (for photophore terminology, see Figure 1) ; however, our five species of Diaphus included were insufficient to validate anything on this matter. One very rare monotypic taxon Idiolychnus urolampus, missing from our study, was transferred from Diaphus to Lobianchia by Bolin  and most lately erected into its own genus Idiolychnus by the position of VO3 and possession of two SAOs .
Gymnoscopelini (clade C) sensu Paxton  was found to be monophyletic although not fully congruent with Ahlstrom et al. . Unfortunately, the monotypic taxon Lampanyctodes hectoris is not included in this study, a myctophid showing ambiguous morphological characters concerning tribal placement. Paxton  noted Lampanyctodes as a possible early divergence based on several characters shared with the most plesiomorphic diaphinid genus Lobianchia. Conversely, Ahlstrom et al.  noted Lampanyctodes as being specialized within Gymnoscopelini from a similar larval form and development to that found within Lampadena, arguing that characters reflect habitat instead of true phylogeny.
Ceratoscopelus and Bolinichthys formed a clade (D) as either sister group to the remaining lampanyctines or included within them (Figures 4 and 5, respectively). Paxton  included these genera within Lampanyctini as closely related, whereas Ahlstrom et al.  placed them within Gymnoscopelini. Our study supports inclusion in Lampanyctini despite unresolved intrarelationships of this tribe. The clade itself is very distinct in terms of mt sequences and supported by both osteology  and larval development .
A tRNA-Glu gene could be detected in the canonical vertebrate position between ND6 and Cytb in all myctophids included in this study, except in a Lampanyctini subclade (E) comprising Stenobrachius, Triphoturus, Nannobrachium and Lampanyctus (Figures 3). In Nannobrachium ritteri and Lampanyctus crocodilus, we were able to determine a novel location of tRNA-Glu in the highly polymorphic region downstream Cytb including the tRNA-Thr and Pro genes, the CR and various INC-regions. Sequence similarities between tRNA-Glu from N. ritteri and L. crocodilus and the INC-regions between ND6 and Cytb were evident from sequence comparisons and putative secondary structures (see Additional file 3). Interestingly, this INC-region showed no sign of redundancy since all five taxa have retained a fragment equal in size to the typical length of tRNA genes (68–73 base pairs). We tentatively assign this gene order to the lampanyctine subclade E and note that this clade is congruent with Paxton  and Paxton et al. , although the latter notes that no synapomorphic character is present to actually define the clade. We expect this feature to be found within the unsampled genus Parvilux as well. A new position of tRNA-Glu and retention of an INC-sequence between ND6 and Cytb has also been found in other vertebrates, e.g. the amphisbaenian reptile family Bipedidae , and seems to be one of the most common gene order rearrangements in vertebrates.
A clade consisting of Lampadena and Taaningichthys (F) is found monophyletic and completely congruent with morphology. Taaningichthys was previously a part of the genus Lampadena although it was separated by Bolin  based on characters such as reduced number of photophores and flaccid body structure. Nafpaktitis and Paxton  noted that Lampadena chavesi, L. dea and L. speculigera were more closely related to Taaningichthys than the remaining species of Lampadena based on expanded neural arches on the anterior vertebrae as found in Taaningichthys. In fact, Paxton  noted that discriminating characters between the two genera were hard to find. Lampadena and especially Taaningichthys are among the largest and deepest living myctophids, with the latter showing reduction of the lateral line and in the number of body photophores. This apparent reductional trend has resulted in one taxon, Taaningichthys paurolychnus, having lost all body photophores although retained the supra- and infracaudal glands. Lampadena yaquinae is found nested within the Lampadena species included and corroborates Paxton  in synonymizing Dorsadena with Lampadena. Likewise, the subgenera Lampadena and Lychnophora proposed by Fraser-Brunner , supported by only an elevated PO4, are not supported from this study. Increased mitogenomic taxon sampling of these two genera is interesting concerning evolution of photophores within these deep dwelling genera showing atypical character states within the Myctophidae .
The tribe Electronini (G), erected from low-leveled PVO and PLO photophores , composes a subset of the tribe Myctophini as recognized by Paxton . Our results clearly support Electronini as a separate tribe  from both DNA sequences and long (>200 base pairs) synapomorphic INC-regions upstream the tRNA-Ile gene (Figures 3 and 5). We recovered a sister relationship of Electronini to the rest of Myctophinae, a result also presented by Paxton et al. , although cladistic analyses of morphological characters failed to recover this result (Figures 2E-F).
The IQM-regions of species included in the genera Benthosema and Diogenichthys (clade H) were peculiar and the IQM-region and WANYC-region of both Electronini and Benthosema-Diogenichthys were highly differentiated compared to all other myctophids. Benthosema glaciale showed new positions of tRNA-Gln and -Met to the downstream region of the WANYC-region (Figure 3) representing a novel gene order in vertebrate mitogenomes. Diogenichthys atlanticus showed an IQMM gene order and the canonical vertebrate gene order was observed within Benthosema pterotum and B. fibulatum. Taxon sampling prevents us from discussing rearrangements for these taxa at this point; however, a close relationship between the two genera is consistent with morphology. Diogenichthys was separated from Benthosema by ventrally leveled Prc 1 and 2 in addition to various jaw differences and hooked dentary teeth, a character state only found within lampanyctines. Similar to Notolychnus, D. atlanticus is a diminutive species with adult maximum size < 30 millimeters and could represent a problematic branch within this clade considering character states related to miniaturization. Diminutive species are also found within the genus Diaphus. The Benthosema-Diogenichthys clade was supported from DNA sequences and an INC-region up- or downstream tRNA-Gly; all three species of Benthosema showed an INC-region flanked by an upstream CO3 gene and downstream tRNA-Gly. In addition, B. glaciale showed an INC-region after tRNA-Gly. In D. atlanticus, however, the INC-spacer was located downstream from the tRNA-Gly gene (Figure 3). Interestingly, two tRNA-Gly genes separated by a large INC-region were observed in this same region in Electrona antarctica, although none of the INC-regions could be shown to have any sequence similarity to each other or to tRNA-Gly. We have assumed an INC-sequence associated with tRNA-Gly as a character state for the Benthosema-Diogenichthys clade, although with reservations. In view of E. antarctica possesing two tRNA-Gly genes we note that an association of this region in E. antarctica, D. atlanticus and Benthosema spp. is plausible and should be elucidated with increased mitogenomic taxon sampling.
The tribe Myctophini was not supported from this study as the sister clade to Electronini, because the single representative of the tribe Gonichthyini (Centrobranchus choerocephalus) included in this study renders Myctophini paraphyletic. We note that broader taxonomic representation of the genera Gonichthys, Centrobranchus, Tarletonbeania and Loweina is necessary concerning phylogenetic position of Gonichthyini within Myctophinae. However, evidence from mt sequences and a unique gene order in part of Myctophini (Figure 5) is consistent with the results from Paxton  stating that”..A number of characters suggest that the Myctophum-Symbolophorus line gave rise to the slendertails [ed. tribe Gonichthyini]..”. Additional evidence for this result comes from the non-monophyly of Gonichthyini based on larval characters  (Figure 2C) and the analyses by Stiassny  and Yamaguchi  (Figure 2E-F) showing Symbolophorus a basal branching within Gonichthyini. This study confidently resolves the genus Myctophum into two different clades from mitogenome sequences and also from a unique gene order involving ND6, tRNA-Glu and Cytb (Figures 3, 5). Myctophum affine, M. punctatum and M. nitidulum (clade I) showed this particular gene arrangement whereas M. asperum and M. orientale showed the typical myctophid gene order also found in Centrobranchus choerocephalus and Symbolophorus californiensis, the latter four forming a well supported clade J (Figures 4 and 5). Two species-groups are currently recognized in the genus Myctophum based on cycloid versus ctenoid scales  corresponding to the two separated groups of Myctophum found in this study. Moser and Ahlstrom  discussed eye shape within Myctophum and noted this genus as difficult to distinguish phylogenetically, with stalked eyes usually absent, although present in e.g. Myctophum nitidulum and M. punctatum corresponding to the cycloid-scaled Myctophum lineage from this study. This result is, however, complicated by stalked eyes also being found in all species of Symbolophorus. Clearly, mitogenome sequences and a unique gene order in the cycloid-scaled species of Myctophum strongly suggest that the two groups are in fact different lineages within Myctophini and that the tribe Gonichthyini is nested within the ctenoid-scaled group. This indicates ambiguous relationships from adult and larval morphology or convergent evolution within Myctophini lineages. Paxton  noted that no additional characters are present within Myctophum to support a split between cycloid- and ctenoid-scaled Myctophum species. The term”near-surface” myctophids has been used for a group of myctophids represented within the genera Loweina, Tarletonbeania, Gonichthys, Centrobranchus, Symbolophorus and Myctophum with most species showing DVM behaviour and most being easily netted in surface layers at night time . Denser taxon sampling within Gonichthyini, and the ctenoid-scaled Myctophini group as recognized from this study, should clarify if DVM patterns and phylogeny are correlated.
Diaphini tRNA-Met pseudogenes
Our included taxa in the tribe Diaphini opens up for a unique empirical case of a putative duplication event that can be observed through time for retention and deletion of various genes/pseudogenes in separate diaphinid taxa. All tRNA-Met pseudogenes were retained with 64–68 base pairs whereas other INC-regions between the tRNA genes in this segment (grey areas in Figure 6) seem to be in the process of being removed. Phylogenetic congruence between the mitogenomic sequences and the diaphinid pseudogenes (Figures 5 and 6, respectively) is clear despite the short pseudogene sequence lengths. Only one other vertebrate group, scarrid parrotfishes, shows a similar pattern of gene rearrangement of the IQM-region and retention of the pseudogene , although the pattern of retention and deletion of INC-regions in parrotfishes is much less pronounced (see Additional file 5). We note that the tribe Electronini and other taxa within the subfamily Myctophinae exhibit gene rearrangements, albeit different in organization, associated with this particular region (Figure 3, see Additional file 4). We acknowledge the missing discussion of this region in the subfamily Myctophinae; however, our results concerning this particular region in Myctophinae awaits increased taxon sampling. Topology testing using the AU-test could not reject a Notolychnini-Diaphini relationship (P=0.407; Table 2) in contrast to morphology, mitogenomic sequences and our NJ-analyses of the INC-regions (Figures 2, 5 and 6, respectively).
We note a third case of various anuran putative duplication events of the tRNA-Met gene  and although this case is reminiscent of the low sequence similarity between the two detected tRNA-Met genes as seen in Notolychnus, the tRNA-Met anticodon is repeatedly detected in anurans making this situation different to lantern- and parrotfishes.
Mt gene order rearrangements in vertebrates
Observations of unique gene rearrangements in Myctophidae, combined with their utility as clade defining synapomorphies, are quite numerous compared to similar findings within other vertebrate groups . It should be noted that whereas mt sequences and gene order rearrangements resolve myctophiform relationships in a highly corroborative manner in this study (Figure 5), taxon sampling and unknown selection on gene order and INC-sequences are problematic when inferring phylogeny. Clearly, gene order rearrangement hotspots are present in vertebrate mt genomes and selective constraints could plausibly show convergent evolution to be the reason in some cases . Almost all gene order rearrangements and INC-regions presented for Myctophidae have also been found within other vertebrate groups. For example, the INC-sequence present between ATP6 and CO3 is found within Gonostoma gracile (order Stomiiformes)  and in various deep-sea anglerfishes . Birds (class Aves) all have a clade-defining rearranged gene order encompassing a fragment ranging from ND6 to the CR , although multiple variations have subsequently occurred on top of this synapomorphy . Plethodontid salamanders show multiple gene rearrangements with likely concerted evolution on duplicated regions . The latter also suggested an INC-sequence between tRNA-Thr and -Pro possibly functioning as an alternative initiation site for replication. All myctophiforms successfully determined for this mt site show an INC-sequence between tRNA-Thr and -Pro, although the length of this spacer in myctophids is highly variable (see Additional file 4). Bakke et al.  postulated a selective advantage as a protein-binding site for this spacer, supported by a conservative motif sequence in codfishes. Concerted evolution on CR-duplicates is also reported from snakes  and mantellid frogs , with the latter strongly indicating recombination associated with the CR in various taxa exhibiting duplication events. Varanids and monitors show events in the variable region upstream of the CR  and acrodont lizards show a QIM gene order . As mentioned, scarid parrotfishes all have an IMQ-gene order showing similar patterns as found in Diaphini, with an INC-sequence (pseudogene) retained upstream the ND2 gene from a putative duplication of tRNA-Met . The latter suggested that the tRNA-Met pseudogene neighbouring ND2 retained a function as punctuation mark for ND2 mRNA processing. Mt tRNA transcriptional efficiency in relation to distance of initiation of replication was explored by Satoh et al. , who found support for highly expressed genes positioned closer to the control region. Selection on INC-regions in relation to bordering genes is an important theoretical caveat when using INC-regions as phylogenetic markers. Satoh et al.  initiated mt gene order comparisons within codfishes (Gadiformes), showing rearranged gene orders and INC-regions in a possible similar fashion to Myctophidae. Most notably one species, Bathygadus antrodes, possessed all of the gadiform rearrangements although somewhat differently arranged from other subclades. This indicates early rearrangement events subsequently modified into presently observed synapomorphic gene orders for specific gadiform clades. The most basal branching in Myctophidae, Notolychnus, shows mt rearrangements such as two tRNA-Met genes and a comparatively large INC-sequence between ATP6 and CO3. These features are either modified or lost in other myctophids. On the other hand, several rearranged gene orders found in various myctophid tribes are not traceable in Notolychnus. Gene order rearrangements within Myctophidae provide a unique example of the phylogenetic utility of mt gene orders and the problems associated with this group of markers.
Mitogenomes from myctophiform fishes provide a unique empirical case of mt DNA sequences and gene order rearrangements that corroborate evolutionary history. Future mitogenomic determination of the 200+ remaining species within Myctophidae will most certaninly increase our knowledge concerning issues associated with gene order rearrangement events and their utility as phylogenetic markers. Multiple different gene orders found throughout the mt genome, utility as phylogenetic markers and the unknown causes and mechanisms associated with gene duplication and subsequent retention and/or removal of sequences, calls for the determination of complete mt genomes over single genes. Our results support the use of osteology and photophores in phylogeny of Myctophiformes, the latter being a very unique feature of any deep-sea group of organisms. Larval ontogeny is also informative albeit difficult to use on higher phylogenetic levels and particularly within the subfamily Lampanyctinae.
No ethical issues
The authors declare that no ethical issues were present for this study.
JYP thanks K. Mabuchi, T. Kon, Y. Yamanoue, M. Nakatani, M. Seimiya, M. Yorifuji, S. Hayeun, M. Takada, M. Kawaguchi, T. Shuto, M. Kato, A. Kinjo, T. Nagasaki, (AORI), K. Sünksen, N. Hammeken, S. Hvass, H. Lund (GN-Pinngortitaleriffik) and all crew onboard R/V Pâmiut.
For providing tissue and access to vouchers we thank Center for Molecular Biodiversity Research (NSMT), M. Moku (AORI), H.J. Walker (SIO), S.W. Knudsen, M. Kragh, T. Menne, P. Møller, J. Nielsen (ZMUC), K. Hartel (MCZ), A.C. Bentley (KU), C. Kenealey (WU), A. Graham (CSIRO), G. Herrera, L. Rodriguez-Grana, (Chile & Uruguay, respectively), J. Paxton, A. Hay (AUS), K-T. Shao, L.Y-C. Liao, P-L. Lin (ASIZP), N.V. Gordeeva (IOGEN). A big thanks goes to H. Endo and N. Nakayama (BSKU) for onboard sampling for this study.
For general logistics we thank G. Langhelle, L. Emdal (ZMUB), L. Lindblom, K. Meland (UIB) and Rudolf Svendsen for contributing UW-photograph.
Two anonymous reviewers and editor provided highly constructive reviews of this manuscript before publication. Funding was provided by JSPS Research grants (17207007, 19207007, and 22370035) and Bergen University Museum Ph.D.- and travel grants for JYP.
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