Enhanced dynamicity: evolutionary insights into amphibian mitogenomes architecture

doi:10.21203/rs.3.rs-4830272/v1

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Enhanced dynamicity: evolutionary insights into amphibian mitogenomes architecture

https://doi.org/10.21203/rs.3.rs-4830272/v1

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Mitogenomes are known for their structural dynamics and the complexity of their rearrangement patterns. However, their utility in metazoan comparative biology has not been fully exploited. Vertebrate mitogenomes are now sufficiently representative to allow the development of more advanced methods for comparing genome architecture. Furthermore, the relatively robust phylogeny of vertebrates at higher taxonomic ranks allows us to infer the patterns of genome evolution accordingly. In this study, using amphibians as an example, we performed data cleaning and manual annotation on 1777 samples from the NCBI and identified 88 rearrangement types, most of which were clade specific. In addition, we quantified genomic changes in an evolutionary framework and obtained stepwise growth curves of the architectural changes. This study provides new perspectives for understanding the evolution of the mitogenomes in amphibians and is expected to facilitate the qualitative and quantitative development of mitogenomes research.

Mitogenome

Comparative genomics

Macroevolution

Gene rearrangement

Complexity

Evolutionary transitions

The mitogenomes architecture, as the structural organization of genetic material, exhibits dynamic properties [1]. It displays remarkable plasticity in individuals [2–4], while taking radically various pathways in diverse lineages. The architectural diversity of the mitogenomes provides a noteworthy dimension for observing the complexity of mitochondria as an open system. This diversity encompasses a broad range of genomic rearrangements, including insertions, deletions, inversions, and transpositions, both within genes and in intergenic regions. These structural changes reshape the genome and influence its functionality, thereby affecting species adaptability and evolutionary trajectories. For instance, significant innovations in metazoans, such as the emergence of multicellularity and bilateral symmetry, are associated with specific changes in mtDNA organization [5–7].

Extensively reorganized mitogenomes in amphibians have attracted considerable interest since 1997 [8]. These intriguing features, such as exceptional enlargement (up to 28.8 kbp) [9], loss and gain of genes [10–12], and the stepwise nature of rearrangement [13], all suggest the hidden diversity of amphibian mitogenomes. Beyond the rearranged genes, the long noncoding region or control region (CR) is also the “hot spot”, not only because of its duplication or triplication [9, 10, 14] but also because the replication fork barrier lying in the CRs can often mediate recombination between duplicated CRs [13].

Across amphibian lineages, independent rearrangements have been observed, leading to the consensus that such reorganization patterns can serve as phylogenetic signals of amphibian evolution. For instance, the LTPF tRNA cluster is considered as a synapomorphic characteristic of Neobatrachia [15]. However, further shuffling within the cluster [11], or the involvement of nad5 gene adds complexity, especially when similar events are found in taxonomically distant groups, such as Afrobatrachia [9]. Moreover, the replication of trnM and the presence of IQMM gene clusters in multiple, distantly related taxa further complicate the picture, as in some cases, these clusters exist as two separate copies rather than tandem repeats [16]. Additionally, intraspecific rearrangement diversity cannot be ruled out, as evidenced in Dicroglossidae [17, 18]. These known and unknown complexities urge us to expeditiously unravel the evolutionary landscape of mitogenomes variations in amphibians.

In light of the decreasing costs of high-throughput sequencing technologies [19], advancements in long-read sequencing [9, 20–22], along with optimized assembly and annotation techniques [23–25], we are now able to explore the mitogenomes architecture in greater depth, thereby examining its evolutionary patterns and trends [26]. In this study, we specifically aimed to investigate the genomic architectural diversity of amphibians. We used NCBI2GO (unpublished) to clean the available data from 1777 samples representing at least 710 species to generate a high-quality dataset. Employing qMGR [27] and qGO (unpublished), we conducted qualitative and quantitative comparative studies within a phylogenetic framework to elucidate the patterns of genome structural changes during amphibian evolution. Our findings revealed a phased growth trend in structural changes, providing valuable insights into the evolution of mitogenomes. These insights also have the potential for uncovering the origin and maintenance of animal biodiversity and broadening the scope of comparative genomics research.

2.1. Cleaning and error checking

Accurate annotation is often a challenge [29]. Despite considerable efforts[30–32], the errors in RefSeq annotations are still too severe for gene organization comparisons [33, 34]. The problem is even worse at NCBI, where a large number of sequences are unannotated [35]. Cleaned datasets are also not always accurate [7, 36, 37]. Therefore, in this study, 2143 mitogenomes retrieved from NCBI Organelle Genome Resources using the search string "Amphibia[ORGN] AND (mitochondrion[TITL] OR mitochondrial[TITL]) AND 10000:50000[SLEN] NOT (RNA [TITL] OR gene[TITL] OR product[TITL] OR mRNA[TITL] OR rRNA[TITL] OR misc_RNA[TITL] OR nuclear[TITL])" on October 11, 2023, were cleaned using NCBI2GO (unpublished), a cleaning pipeline developed by the authors. In this pipeline, the gene order was extracted, and the intergenic length was calculated based on the location information to identify the control region (CR) by the threshold. A total of 2143 mitogenomes, including 366 from RefSeq, have been deposited in the GenBank mitochondrial database. 369 out of 1777 samples with missing annotations and those with unconventional gene order were entered into the re-annotation module. Manual verification was then performed to further ensure the reliability of the dataset. For the standardization, the gene nomenclature in [38] is used. The single-letter amino acid codes designate the corresponding transfer RNA genes (trns). L1, L2, S1, and S2 indicate trns for Leu (UUR), Leu (CUN), Ser (UCN), and Ser (AGY), respectively.

2.2. Taxonomic reconciliation

Coherence between species names and their parent taxa is central to comparative analysis at higher taxonomic levels. The NCBI taxonomy was checked against an authoritative list of accepted species. We chose to initially base this comparison on AmphibiaWeb (AW), which contains 77 families with 569 genera and 8689 species downloaded on January 13, 2024 [39].

The 1777 samples were first de-duplicated based on NCBI taxonomy, yielding a list of 97 unidentified species samples (17 with “cf.”, 79 with “sp.”, and 1 unisexal lineage), 1 hybrid, and 40 with “aff.”, 695 species, and 13 subspecies. Matching of the last three of the above five cases

returned the scientific names of 716 species, and the remaining 32 were manually matched to the GBIF Backbone Taxonomy [40]. After the final deduplication, our taxonomic matchup placed 1777 samples into 710 species of 244 genera and 65 families as showed in an additional Table 12.

2.3. Quantification of mtDNA rearrangements

The mitogenomic structural changes can be analyzed quantitatively by calculating the pairwise distance between the rearrangements and the ancestral organization. We applied both the qMGR [28] and qGO algorithms separately to the above dataset. While both aim to quantify the rearrangement frequency (RF) of each individual gene and the rearrangement score (RS) of each mitogenome, qMGR is alignment free, which calculates the RF of a given gene by accumulating the changes in the two nearest neighboring genes. However, qGO, developed by the authors (unpublished), relies on homology alignment to calculate the RF of the target gene directly. It also supports weighting, so breakpoints need to be predefined to generate intervals that give weight to genes that translocate across the interval. Following the widely accepted processes of replication [41] and transcription [42, 43], we set OriL and OriH as the two breakpoints that force the circular genome into two intervals. The genes within each interval are then manually aligned separately as the input for qGO.

2.4. Evolution of mitogenomic structures across amphibians

The time-calibrated molecular phylogeny of Jetz and Pyron [44] was used for comparative analyses. Changes were made to update families (Hynobiidae, Ambystomatidae, Proteidae, Rhyacotritonidae, Amphiumidae, Plethodontidae, Ascaphidae, Alytidae, Rhinophrynidae, Scaphiopodidae, Megophryidae, Limnodynastidae) and prunes (Odontobatrachidae, Conrauidae, Nyctibatrachidae, Ceuthomantidae, Cycloramphidae, Batrachylidae, Allophrynidae) due to the updata and the lack of complete mitogenomic data. All types are first projected to the phylogeny, and the ancestral type for the diversity is inferred to be the relative outgroup.

3.1. Overview of mitogenomic organization in amphibians

Numerous errors in the annotation were identified and reviewed. Error types include but are not limited to abnormal reading direction (strand), erroneous gene designations, missing gene or other feature annotations, mistaken identity of trnL1/trnL2 and trnS1/trnS2 tRNAs, and inconsistencies in gene names. The most misleading situation is when the errors were included in RefSeq [45]. After data cleaning, error checking and taxonomic reconciliation, we obtained a dataset containing 1777 samples representing 710 species in 244 genera under 65 families, yielding 88 gene rearrangement types (Table S1). Species coverage within each genus was variable, with a mean of 35% and a median of 25%. Among them, Caudata was the richest (mean 58%, median 50%), and Neobatrachia was the least abundant (mean 23%, median 13%) (Fig. 1 and Table S3).

The unexpected complexity and variability among amphibian mitogenomes were revealed (e.g., Fig. 2 and Table S2). The major lineages of both Gymnophiona and Archaeobatrachia, as well as a few Caudata, were identical to the typical vertebrate gene order (orange circle in Fig. 1a), which was named the Amphibian ground pattern herein and labeled type 1 in additional tables. In addition, both Caudata and Neobatrachia have their own autapomorphies. The Caudata ground pattern (type 2, red circle) features one more CR derived between trnT and trnP. The Neobatrachian ground pattern (type 21, blue circle) has a strongly rearranged gene order, involving the long-term translocation of trnL1 to form the LTPF tRNA gene cluster located upstream of the 12S rRNA gene [46].

In contrast to all 10 Caudata families, which have consistently retained the ground pattern among their members, only 24 of 35 Neobatrachia families show the Neobatrachia ground pattern. Among these, 9 families have evolved new types. The remaining 11 families exhibited completely derived types, leading to a total of 69 rearranged types. This makes Neobatrachia the most variable group, followed by Archaeobatrachia with 10 types, Caudata with 8, and Gymnophiona with 5, as shown in Fig. 2a.

The most common rearrangement events observed in this study involved nad5, trnTP, trnL1 and CR [46]. Inversions are rare relative to translocations. Notably, consistent with findings from long-read sequencing, multiple rearrangement types involved duplication of genes or gene clusters, as well as repetition of CR or a combination of both [47]. Among them, trnM duplications were the most common, followed by trnP duplications, as detailed in Fig. 2b and Table S2.

3.2. Mitogenomic structural changes across four lineages

Mosaic evolution and lineage specificity coexisted throughout mitogenome evolution in amphibians. In particular, the ground patterns of vertebrate (n = 162) and Caudata (n = 415) are shared among distantly related species of Gymnophiona, Caudata, and Archaeobatrachia. However, both patterns are notably absent in Neobatrachia. Moreover, the 67 derived types that evolved from the Neobatrachian ground pattern (n = 756) are unique to this lineage and are not observed in the other three lineages. These observations challenge our understanding of the organization of the ancestral amphibian mitogenome. Both Rhinatrematidae and Ichthyophiidae (Uraeotyphlus only), the two most basal families of Gymnophiona, possess the Caudata ground pattern [48]. Given the rearrangements found in Caudata and Archaeobatrachia, it is difficult to rule out the possibility that the ancestral state of the amphibians was a Caudata ground pattern. However, the majority of Gymnophiona, with the exception of the aforementioned families, exhibit this vertebrate pattern. Therefore, applying the principle of parsimony, the most plausible hypothesis is that the ground pattern of amphibian mitogenomes is a vertebrate pattern.

Almost all mitogenomic structural changes in Gymnophiona are genus specific, except for Boulengerula, which has interspecific variation, with one of the two species having a duplicated trnP (Type 3). There are also two types (types 4 and 5) concentrated in the trnWANCY clusters that are restricted to two genera in Siphonopidae. The Caudata ground pattern is shared by all 10 Caudata families, yet two of them have derived taxa. Among the 168 Caudata species examined, there is intrageneric differentiation in the genus Tylototriton, and two of these species are type 11, involving the expansion of the CR and its flanking genes [14]. The seven Plethodontidae species from Tylototriton, Aneides, Hydromantes and Plethodon are all intragenerially diverse to types 6–9, and the single-sample Stereochilus is type 10. Archaeobatrachia comprises four successively evolved lineages, all of which can be traced back to the ancestral amphibian type. Two out of four genera of Pipidae, Pipa and Xenopus, possess both Type 1 and Type 2. Derived types 20 (swaps of nad6-trnE and cob-trnT) were found in both examined species of Leiopelmatida. The more diverse Megophryidae show an additional seven derived types occurring in Leptobrachium (Type 14), Leptobrachella (Type 13) [49, 50], Scutiger (Type 17) [51] and Oreolalax [49, 52, 53], which intragenetically diversified into five derived types. These changes primarily involve the duplication of trnM [46] and/or the remote transposition of trnW.

There is very high variation in the genomic structure of Neobatrachia. Whether derived in terms of majority rules or the status of the outgroups, the ancestral type should contain a unique rearrangement in which trnLTP forms a cluster of genes located between the CR and trnF. In addition to type 21, which is shared by 24 families and is therefore considered to be the ground pattern, there is another type shared by four distant families (type 48), which differs from the ground pattern only by an additional CR between nad5 and nad6. Another pair of sister groups shares type 27, which has an additional interchange of trnA and trnN on top of the ground pattern. The remaining 66 types other than these three are unique to a given family, meaning that they are no longer shared between families [46]. The clade comprising Dicroglossidae [17, 46, 54–56], Ranidae [55, 57–63] and Rhacophoridae [64–66] exhibits the strongest changes, encompassing nearly half of the derived types (32 in total) with Breviceps, Hyperolius, Ptychadena, Cornufer, Limnonectes, Amolops, Nidirana, Odorrana, Rana, Polypedates, Nanorana, Quasipaa, and Nanorana presenting intrageneric changes and the latter two even presenting intraspecific changes [17, 18]. Nested within this clade, Mantellidae and Ranixalidae each harbor family-specific types. Other intrageneric changes occur in Cornufer, Ptychadena [67], Hyperolius [9], Breviceps [9, 68], Ischnocnema [69], Brachycephalus, Boana, and Bokermannohyla and reach an extreme of nine types in Pristimantis. The changes are varied and involve almost all regions of the mitochondria. The most notable variable regions involved the tRNA gene cluster WANCY [70]; in particular, multiple OLs were identified in the clusters [71].

3.3. Quantitative analysis of mitogenomes changes across amphibians

The hotspot is depicted in Fig. 1b on the heatmap plotted against the relative frequency (RF), detailed in additional table S5. Each amphibian group is represented by a different color, with purple indicating the entire amphibian group. The gradient of color shading reflects the relative RF score. Among all the genes, trnL1 exhibited the highest score due to its long-range translocation across various amphibian taxa. However, when examined at a finer taxonomic level, trnL1 rarely undergoes changes within that specific taxon. It should be noted that hotspots differ between taxa. For instance, Gymnophiona primarily experiences changes in the trnWANCY gene cluster, while Archaeobatrachia scores highest for the flanking genes of nad2. Neobatrachia displayed significantly more variable regions than did the other taxa, with almost all the genes exhibiting some degree of rearrangement except for cox2, atp6, and nad4l, which had RF scores of 0. Notable hotspots common to all three taxa may be confined to the region between nad6 and trnF, including CR [16].

Further analysis of the RS distribution (Fig. 1c and Table S2) highlighted the significant variation in mitogenomes architecture among amphibians. Gymnophiona, the most primitive group, exhibited the lowest median RS intensity, suggesting a relatively low level of genomic change. Caudata has a greater median RS than Archaeobatrachian, possibly due to Pyxicephalus adspersus, which undergoes strong rearrangement with gene duplication, resulting in 49 genes [12]. This extreme value elevates the overall distribution profile with score peaks at 50 (qGO) and 46 (qMGR). However, disregarding this extreme value, both taxa exhibited relatively uniform distributions of RS that were generally greater than those observed in Gymnophiona. It is worth noting that although both Caudata and Archaeobatrachia had a minimum RS value of 0, considering that type 1 in Cadauta evolved from ancestral type 2, this score varied when type 2 was changed to the reference. The multimodal distribution observed in both Archaeobatrachia and Neobatrachia indicates heterogeneity, potentially suggesting divergent evolutionary directions. A more intriguing alternative inference concerns the emergence of Neobatrachia, which disrupts continuity and gives rise to fluctuations in Archaeobatrachia. Neobatrachia, as the most recently evolved lineage, stands out for its high RS values and several extreme values. There are ten values above 20, a magnitude that far exceeds that of any other taxon, suggesting that it may have evolved in an aggressive way, avoiding the fatal decrease in evolutionary potential. This is consistent with the evolutionary pattern observed in other vertebrates, where more recently evolved taxa tend to have greater complexity. The extremely high RS may also indicate that the taxa have undergone rapid adaptive radiation or evolutionary innovation, resulting in significant increases in complexity.

3.4. Evolutionary dynamics underlying patterns of diversification

By aligning the RS of each taxon with the time of origin of its corresponding branch and aggregating the RS values over time, a growth curve can be generated (Fig. 3 and Table S5). A comparison between the growth curves for all amphibians and those for each individual taxon revealed a consistent pattern of stepwise growth over time. This suggests that there were distinct periods of rapid expansion followed by relatively stable phases in amphibian evolution.

Interestingly, while the absolute values of RS exhibited considerable variation across taxa, they demonstrated remarkably consistent patterns of increase, except for Gymnophonian, which consistently experienced a step change during the Cretaceous period. This indicates that Gymnophiona underwent unique evolutionary events or adaptations during this specific period. Furthermore, when examining the remaining three branches, it becomes evident that they all display a rapid increase with nearly comparable slopes soon after the beginning of the paleogene. This sudden surge in their RS values is preceded by an extended period of stagnation and a minor, limited magnitude increment occurring around or prior to the mid-Cretaceous epoch. The long periods of silencing in the early clade may indicate an underestimation of potential diversity for various reasons, such as extinctions associated with specific rearrangements.

4.1. Unraveling the complexity: mitogenomes variability in amphibians

The dogma that there is a frozen mitogenomes in vertebrates has long been broken, but vertebrates are still considered subphyla with probably the lowest variability in mt DNA gene content and gene order, with disparities thought to have a limited taxonomic distribution. This frosted glass exists mainly because of uneven sampling [72], a high percentage of erroneous annotations [33] and problematic mitogenomes [34], as well as the omission of duplicated regions [73]. During the last few years, the advent of high-throughput sequencing techniques has increased the number of sequenced mitogenomes. Vertebrates, in particular, account for more than half of all Metazoa [7]. Specifically, for amphibians, an adequate representation of 88% of the families is sufficient to infer consensus mitogenome characterizations of different taxa and to fully recognize exceptions that lie beyond this consensus. The present study revealed that 43% of the amphibian genera examined had at least one available mitogenome. However, the data still suffer from taxon bias. In the case of Gymnophiona, mitogenomic structural changes often occur at the genus level. The lack of novel rearrangements, despite a genus-level coverage of 82%, suggests data saturation. Conversely, although the number of Archaeobatrachia mitogenomes exceeds that of Gymnophiona mitogenomes, changes could occur within genera even within species, suggesting that as species diversity increases, the emergence of new types of mitogenomes is possible. In other words, the existing data for Archaeobatrachia may be insufficient [49].

The mitogenomes, traditionally considered highly conserved, exhibits unexpected dynamism, with 88 observed types in our study. This diversity, however, is likely an underestimate, suggesting that the complexity of the mitogenomes extends beyond current comprehension, especially when considering regions of high variability [13, 47] that were excluded from this dataset due to stringent search criteria. In a phylogenetic framework, structural diversity is sensitive to the grain of phylogenetic resolution. Specifically, the differences between major types (type 1 and type 2) in amphibians, birds and reptiles [23, 74] hinge on the presence of an additional CR between trnTPs, and Neobatrachia shows phylogenetic constraints from ancestral type 21. In contrast to the path-dependent evolutionary trajectories described above, fine-grained taxonomic diversifications appear to be stochastic and unpredictable, underpinning the individualized nature of mitochondrial evolution within specific families, [75] as depicted in Fig. 1a. These changes involve all kinds of components, including tRNAs, protein-coding genes, rRNAs, and the CR, occurring regardless of the gene position relative to the CR and affecting both strands.

This observation challenges the prevailing notion of convergent evolution in vertebrate mitochondrial gene rearrangements, suggesting instead that the forces shaping mitochondrial genomic organization are diverse and influenced by unique evolutionary histories [36, 76]. Based on such observations, it is reasonable to hypothesize that a variety of mechanisms can drive mitogenome structural changes, extending beyond the duplication-random loss (DRL) model traditionally invoked to explain genomic alterations [77–79]. The DRL model, while useful in explaining certain types of genomic changes at the individual level, may not fully account for the broad variability observed across different lineages [46, 80] or proclivity, such as nested copies of duplicated segments [68]. This raises critical questions about the underlying mechanisms that confer flexibility and robustness to mitogenomes evolution, thereby enhancing its evolvability.

4.2. An asynchronous symphony of the episodic architecture variation

Complexity often emerges from an intricate dance of genetic and environmental factors, resulting in the quantification of features that exhibit fluctuations across multiple dimensions. Through the use of RS and RF as proxies for measuring complexity, genetic innovations can be traced step by step, and amphibian evolution dynamics can be linked to genomic structure evolution. As shown in Fig. 1c, primitive taxa tended to exhibit simpler structures and lower levels of RS, while derived taxa, on the other hand, showed a significant increase in RS across several levels. This increase in complexity suggests that the genomic structure is able to evolve, enabling the exploration of new strategies and facilitating diversification [81]. In other words, evolvability evolved [82]. The case of Archaeobatrachia sheds further light on how this trend impacts specific groups within these taxa. The fluctuating RS suggests that Archaeobatrachia may have undergone a phase of complexity reduction or macroevolutionary freezing [83], which is precisely a consequence of the evolution of evolvability [84].

Rearrangement frequency (RF) helps us understand complexity by showing that genes or gene clusters within a genome may undergo independent evolution [85, 86]. The trnW gene was used as an example. Although its overall RF appears normal across various amphibian groups, a zoomed-in examination revealed heterogeneity. Within Archaeobatrachia, all types involved trnW shifts, resulting in a remarkably high RF. In contrast, RF rapidly decreased in Gymnophiona but reached zero in Caudata. The heterogeneous behavior of gene rearrangement challenges the notion that the mitogenome evolves as a cohesive, inseparable evolutionary unit. It becomes evident that the way a genome evolves depends on the distinct patterns of independent evolution present among the different genes or gene blocks that a particular genome contains [87].

By examining changes in RS over time, it is possible to trace the increasing complexity of genomic structures and to infer the reasons for this complexity. As shown in Fig. 2, across multiple time intervals, we observe a pattern where periods of stasis are punctuated by brief bursts of rapid evolution. The concept that the rate and pattern of evolutionary change are closely linked to selective pressures at the lineage level is a longstanding and vital part of macroevolutionary theory [88], and this concept also applies to mitogenomic evolution [89]. However, the episodic increase in the number of salientians (anurans and caudates) showed a similar pattern at significant timescales. The first increase, which was very small and occurred at the beginning of the Jurassic, was followed by an increase in limited growth near the Jurassic and Cretaceous boundaries, and a third significant increase occurred just after the K-Pg line, overlapping with the rapid diversification of species-rich clades [90, 91]. Between these periods of growth are long periods of stagnation, which may reflect temporarily rising ‘challenging times’ for diversification of mitogenomes, possibly due to evolutionary constraints. The generalizability of this pattern across different amphibian clades highlights the dynamic nature of mitogenomes and the intermittent nature of the evolutionary events that shape their structure. Episodic mitogenomic evolution is also evident in other metazoans, such as fish and invertebrates [92] In these organisms, drastic changes in mitogenomic structure have been linked to episodes of adaptive radiation [93] or extreme environmental adaptation.

The complexity and evolvability of amphibian mitogenomes structure could be shaped over evolutionary time by various external forces [94]. These forces include not only the deterministic effects of evolutionary events but also the stochastic influence of random changes. This interplay of factors has endowed mitogenomes with a capacity for adaptation and innovation that exceeds the predictions of traditional evolutionary models. The evolvability of mitogenomes through gene rearrangements highlights the dynamic role of genome structure in shaping the evolutionary trajectories of organisms. In addition to serving as repositories of genetic information, mitogenomes actively participate in evolutionary processes by responding to selective pressures and environmental challenges through structural changes.

We collected and curated all available mitogenomes for amphibians and discovered the unexpected dynamism of their architecture. The quantification of structural changes reveals the episodic pattern and highlights the diversity in terms of lineages and genes. This study sheds light on the mechanisms driving genome evolution and underscores the importance of genome structure in shaping the evolutionary fate of organisms. We challenge the simplistic view of genetic structural changes as discrete qualitative units and emphasize more specific quantitative descriptions of patterns of genome structural evolution.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Availability of data and materials

The data and materials presented in the study are included in the article/ Supplementary Material. Further inquiries can be directed to the corresponding author.

Competing interests

The authors declare no competing interests.

Funding

This research was supported by the National Natural Science Foundation of China (31970447; 32370500).

Authors’ contributions

Y.X.: Formal analysis, Writing, Original draft preparation, Visualization. G.N.: Conceptualization, Methodology, Validation, Writing, Reviewing and Editing. H.S.: Software, Data curation. Z.W.: Investigation. R.D.: Formal analysis. Y.L.: Resources. M.W.: Supervision, Project administration, Funding acquisition.

Acknowledgements

The members of the Lab of Insect Systematics and Evolutionary Biology (LISEB) at Jiangxi Normal University are thanked for their contributions to laboratory work. The authors thank Jia-Yong Zhang and Jin Che for the assistance with revision. We thank the anonymous reviewers for their careful reading and many constructive comments.

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Enhanced dynamicity: evolutionary insights into amphibian mitogenomes architecture

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Version 1

Abstract

Figures

1. Introduction

2. Materials and methods

2.1. Cleaning and error checking

2.2. Taxonomic reconciliation

2.3. Quantification of mtDNA rearrangements

2.4. Evolution of mitogenomic structures across amphibians

3. Results

3.1. Overview of mitogenomic organization in amphibians

3.2. Mitogenomic structural changes across four lineages

3.3. Quantitative analysis of mitogenomes changes across amphibians

3.4. Evolutionary dynamics underlying patterns of diversification

4. Discussion

4.1. Unraveling the complexity: mitogenomes variability in amphibians

4.2. An asynchronous symphony of the episodic architecture variation

5. Conclusions

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1