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Full Research Article

Phylogenetic Insights from the Mitochondrial Genome of Eothenomys olitor (Thomas, 1911): A Cricetidae Perspective

Juan Zhang1, Chengyao Yang1, Chaoyang Luo2, Wanlong Zhu1,*, Yuan Mu2
1Key Laboratory of Ecological Adaptive Evolution and Conservation on Animals-Plants in Southwest Mountain Ecosystem of Yunnan Province Higher Institutes College, School of Life Sciences, Yunnan Normal University, Kunming-650 500, China.
2Institute of Eastern-Himalaya Biodiversity Research, Dali University, Dali-671 003, China.

ABSTRACT

Background: The mitochondrial genome serves as a pivotal molecular marker for delving into systematic relationships and adaptive mechanisms. The genus Eothenomys (Cricetidae: Arvicolinae) has consistently attracted attention due to its similar biological characteristics and the analysis of its mitochondrial genome offers a fresh perspective for comprehending the phylogeny and adaptation within Cricetidae.

Methods: We sequenced and analyzed the entire mitochondrial genome of E. olitor and utilized the 13 PCGs derived from this genome to delineate the phylogenetic relationships within the Cricetidae and further evaluated the evolutionary rate of each PCG.

Result: The findings revealed that the mitochondrial genome of E. olitor was 16,351 bp in length, including 13 PCGs with ATN initiation codons, 22 tRNAs, 2 rRNAs and 1 D-loop. Apart from the nad6 and 8 tRNAs positioned on the J-strand, the majority of the genetic elements were situated on the N-strand. The phylogenetic examination yielded a robust phylogenetic tree for Cricetidae, but the placement of some genera remained contentious, which needs more integrative and effective data. Among of them, E. olitor was a sister of E. chinensis and Eothenomys was monophyletic. Moreover, a selective analysis showed that evolutionary rates are significant differences among the 13 PCGs. Among these genes, atp8 a high evolutionary rate, while cox1 has a low. This research uncovered the mitochondrial genome analysis of E. olitor, offering valuable perspectives the phylogeny and adaptation within Cricetidae.

INTRODUCTION

Cricetidae, one of the largest families in mammals, was also an extremely diverse group of rodents, which result in the diverse and complex classification and phylogeny (Wilson and Reeder, 2005). This lineage was abundant in a variety of habitats, including grasslands, shrubberies, hills or plains and others. Previous research suggested that Cricetidae species distributed in China can be divided into four main subfamilies: Cricetinae, Gerbillinae, Myospalacinae and Microtinae/Arvicolinae (Luo et al., 2000). However, due to different taxonomic views, limited specimens and the large increasing number of species, the classification of extant Cricetidae has been always changing. According to the latest view, Gerbillinae cluster with Muridae and Myospalacinae with Spalacidae, because their morphological traits and habits were significantly different from those of other Cricetidae species (Wilson and Reeder, 2005; Ding, 2017). The taxonomic position of Arvicolia has been always discussed, some were support (Abramson et al., 2021; Wang et al., 2022) and some were against (Steppan and Schenk, 2017; Liu et al., 2017). Additionally, Pavlinov and Lissovsky (2012), Wilson et al., (2017) and Liu et al., (2017, 2020) confirmed that the genus status for Alexandromys, Crazeomys rather than subgenus. The genus Eothenomys, found in the Hengduan mountain regions and adjacent areas, has exhibited rapid adaptive evolution during adaptive radiation. In recent years, more and more new species was identified (Zeng et al., 2013; Tang et al., 2021; Wang et al., 2022). However, the absence of effective molecular markers has resulted in the phylogenetic trees have poor resolution and the interrelationships are controversial (Martínková and Moravec, 2012; Fabre et al., 2012; Wang et al., 2022). Notably, even the phylogeny of Cricetidae has been paid more and more attention, including species, genera, tribes and subfamilies (Teta et al., 2017; Liu et al., 2018; CastañedaRico et al., 2023), it still remains controversial. Therefore, there was an urgent need for more effective molecular markers to further investigate the phylogenetic and evolutionary relationships of the genus Eothenomys and its Cricetidae.
       
Mitochondrial DNA (mtDNA) was the most efficient and sensitive phylogenetic marker (Ding et al., 2016; Kiraz et al., 2024). Specifically, mtDNA evolved separately from nuclear DNA and has the characteristics of maternal inheritance, conservative organization and high evolutionary rate, thus, it has always been used for phylogenetic construction and population genetic differentiation and other related studies (Xin et al., 2017; Wang et al., 2018). Additionally, complete mitochondrial genome datasets provide robust insights into phylogenetic relationships (Xin et al., 2015; Wang et al., 2021).
       
In this research, we successfully conducted the entire mitochondrial genome analysis of E. olitor and subsequently utilized the 13 PCGs to elucidate the phylogenetic relationships within the Cricetidae. Furthermore, we have conducted a detailed examination of the evolutionary rates across these PCGs. The objectives of our research are two-fold: (1) decipher the mitogenomic structure of E. olitor and (2) investigate its phylogenetic position and adaptive traits within Cricetidae.

MATERIALS AND METHODS

Sample collection, DNA extraction and sequencing
 
The research samples were collected in May 2023 at the Dashanbao Black-necked Crane National Nature Reserve in China (Fig 1) and then sent to Yunnan Normal University for a one-year study. The liver samples were preserved in 100% ethanol before being dispatched to Shanghai Personalbio Technology Co. for the genome extraction and sequencing. The general steps were as follows: Firstly, the total DNA of the liver was extracted by the improved CTAB method and then its quality and concentration were detected using the Thermo Scientific NanoDrop 2000 and agarose gel electrophoresis. Secondly, the qualified DNA was used to construct a library with various insert fragments of 400 bp utilizing the Whole Genome Shotgun (WGS) approach, followed by Paired-end sequencing (PE, 2×150 bp) using Illumina NovaSeq Next-generation sequencing (NGS). Thirdly, data quality control was conducted using Fastp (Chen et al., 2018) to obtain high-quality sequences. Fourthly, the sequence was assembled and identified using a suite of bioinformatics tools: A5-miseq v20150522 (David et al., 2014), SPAdes v3.9.0 (Bankevich et al., 2012), Mummer v3.1 (Delcher et al., 2003) and Pilon v1.18 (Walker et al., 2017) to deduce the definitive mitochondrial sequence. Subsequently, submit the sequence to NCBI (GenBank accession number: NC_086591).
 

Fig 1: Sampling site of E. olitor.


 
Sequence annotation and analyses
 
Following the splicing process, the refined sequence was deposited to the MITOS (http://mitos.bioinf.uni-leipzig.de/) for functional annotation and download tRNA to check its predicted secondary structures (Matthias et al., 2012). Additionally, we conducted an analysis of the base composition and skewness across the whole genome, PCGs and rRNAs utilizing the PhyloSuite v1.2.3 (Zhang et al., 2020). The strand asymmetry indices were derived using established formula (Nicole and Thomas, 1995; Hassan et al., 2023). The entire mitochondrial genome's structure was visually represented utilizing the CGView (Paul and David, 2005).
 
Phylogenetic and selection analyses
 
To investigate the position of E. olitor and the phylogenetic relationships of Cricetidae, mitochondrial genomes from 22 genera of Cricetidae were obtained, complemented by outgroup representatives from Muridae and Spalacidae sourced from NCBI (Table 1). The phylogenetic tree was then constructed based on 13 PCGs from 98 species employing Maximum Likelihood (ML) methods in PhyloSuite v1.2.3, resulting in a single topology with robust support (Zhang et al., 2020). This tree wasconducted in IQ-TREE (Nguyen et al., 2015), with bootstrap values (BS) above 75% considered significant, indicating higher reliability the topology (Wang et al., 2023). Subsequently, the definitive trees were rendered and refined with the assistance of FigTree v1.4.4 (http://tree.bio.ed.ac.uk/software/Figtree/).
 

Table 1: The species name and ID number retrieved from NCBI.


       
To evaluate selective pressures acting on 13 PCGs across 98 species, we utilized Code ML in PAML v4.9 (Yang, 2007) to determine the evolutionary rates via the free-ratio model (dN/dS). To statistically test for variations in evolutionary rates among the 13 PCGs, we extracted the dN/dS ratios for all species. Subsequently, a one-way ANOVA analysis using the R software (https://www.r-project.org/) to identify significant differences in it. Notably, to ensure the validity of the statistical analysis, data points where dN or dS was zero and where dN/dS was greater than or equal to one, were specifically excluded.

RESULTS AND DISCUSSION

Genome structure, composition and skewness
 
The mitochondrial genome of E. olitor was fully sequenced, measuring 16,351 bp, following a typical rodent structure. It consists of 13 PCGs, 22 tRNAs, 2 rRNAs and 1 D-loop (Table 2, Fig 2). Notably,1 PCG (nad6) and 8 tRNAs (trnQ, trnA, trnN, trnC,trnY, trnS2, trnE, trnP) were positioned on the J-strand, while the majority of genetic elements were on the N-strand (Table 2). The genome¢s nucleotide composition showed A + T content at 59.09% and G + C content at 40.91%, the former was significantly higher than the later. Except nad4l, nad6 and OH, the AT_skew was predominantly positive. Conversely, except OL and nad6, the GC_skew was predominantly negative. The smallest AT_skewwas nad4l (-0.06) and the largest was OL (0.273). The smallest GC_skew was nad2 (-0.593) and the largest was nad6 (0.538) (Table 3).
 

Table 2: Correlation analysis of mitochondrial genome features in E. olitor.


 

Fig 2: Mitochondrial genome structure loop map of E. olitor.


 

Table 3: The base composition and skewness of whole genome, PCGs, rRNAs of E. olitor.


 
PCGs, tRNAs and rRNAs
 
The 13 PCGs in the E. olitor include nad1-6 and nad4l, atp6 and atp8, cox1-3 and cytb. The size varies from 204 bp (atp8) to 1812 bp (nad5).PCGs typically begin with ATN codons (ATA, ATC, ATG and ATT) and with TAN codons (Table 2), consistent with other Eothenomys as documented in previous researches (Yang et al., 2012; Chen et al., 2015; Mu et al., 2019; Zhu et al., 2023). Except nad4l and nad6, the skewness of the majority of genetic elements predominantly favors As and Cs, reflecting a nucleotide compositional bias (Table 3). Meanwhile, E. olitor has 22 tRNAs, varying in size between 59 bp (trnS1) and 75 bp (trnL2) (Table 2). Notably, the trnS1 lacks the dihydrouridine (DHU) arm, while other genetic elements can from the cloverleaf structure. In addition to the normal base pairing, G-U pairing exists in 10 tRNAs (trnR, trnN, trnQ, etc) (Fig 3). The rrnS and rrnL are positioned on the N-strand, separated by trnV (Table 2), with the highest A + T % content (Table 3).
 

Fig 3: The secondary structure chart of 22 tRNAs in E olitor.


 
Phylogenetic and selection analyses
 
This research examines 13 PCGs across 98 species utilizing ML methods to reconstruct phylogenetic relationships. The resulting tree had strong support, with most nodes having BS values over 75% (Fig 4). The analysis showed E. olitor as a sister of E. chinensis and the genus Eothenomys was monophyletic, divided into two main lineages: (E. eleusis, E. miletus, E. cachinus, E. melanogaster) and (E. olitor, E. chinensis).This classification aligns with previous studies by Liu et al., (2012, 2018) and Wang et al., (2022). Concurrently, Neodon, Microtus, Peromyscus, etc., were also monophyletic. However, some genera in Cricetidae were paraphyletic, especially Myodes and Cricetulus, aligning with findings by Liu et al., (2019), Tang et al., (2021) and Wang et al., (2022), but different from Martínková and Moravec (2012). Notably, the phylogeny of Cricetidae remains controversial due to adaptations to diverse environments, variations in evolutionary rates among lineages, inconsistencies in DNA markers and unresolved node. For example, the phylogeny proposed by Wang et al., (2022) (6517 nucleus genes, 122 taxa) supports the monophyletic status of Arvicolinae, including Microtus. Conversely, the phylogeny of Arvicolinae by Martínková and Moravec (2012) (mitochondrial and nuclear DNA) indicates the paraphyly of Microtus. The phylogenies reconstructed by Luo et al., (2004) and Elena et al., (2008) for Arvicolinae using cytb tentatively position Ondatra as a sister of Arvicola, contrasting with our research. Consequently, future research on Cricetidae necessitates the use of effective molecular markers and comprehensive sampling to enhance our understanding of their phylogenetic relationships.
 

Fig 4: Phylogenetic tree inferred from 13 PCGs of 98 species by using ML.


       
Organisms frequently evolve adaptive mechanisms to survive, focusing on energy metabolism crucial in various environments. Mitochondrial genes have attracted much attention for their selective role in adaptive evolution because of its crucial function on energy metabolism (Wu et al., 2022). The selection analysis showed atp8 has high dN/dS average values, indicating accelerated evolution or relaxed selective constraint, which is consistent with research on other species like Orthoptera insects (Chang et al., 2020) and Lamprologus (Wang et al., 2023). In contrast, cox1 has low dN/dS average values, suggesting stronger evolutionary constraints (Li et al., 2021) (Fig 5). Therefore, cox1 and genes with similar constraints are commonly used for phylogenetic reconstructions. Additionally, there were significant differences (P<0.05) in the evolutionary rates of the genes (Fig 5).
 

Fig 5: Boxplot of dN/dS of the 13 PCGs from 98 species.

CONCLUSION

The current research represents the initial comprehensive sequencing and in-depth analysis of the entire mitochondrial genome of E. olitor and the phylogenetic position was assessed using ML methods, offering a fresh perspective for the phylogenetic and adaptive studies within the genus Eothenomys and Cricetidae. However, disagreements persist regarding the classification and placement of genera like Myodes, Cricetulus and Ondatra within Cricetidae. Therefore, there were critical needs for more comprehensive and efficient data to enhance understanding of the phylogenetic and evolutionary relationships among Cricetidae genera.

ACKNOWLEDGEMENT

This work was financially supported by the National Natural Scientific Foundation of China (32160254, 32360119), Yunnan Fundamental Research Projects (202401A S070039), Yunnan Ten Thousand Talents Plan Young  and Elite Talents Project (YNWR-QNRC-2019-047).
 
Ethical approval
 
All animal procedures were within the rules of Animals Care and Use Committee of School of Life Sciences, Yunnan Normal University. This study was approved by the committee (13-0901-011).

CONFLICT OF INTEREST

All authors declare that they have no conflicts of interest.

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