The first complete mitochondrial genome of a trichodactylid crab: Rodriguezia adani (Brachyura: Trichodactyloidea: Trichodactylidae) from Mexico
Primer genoma mitocondrial completo de un cangrejo tricodactílido: Rodriguezia adani (Brachyura: Trichodactyloidea: Trichodactylidae) de Mexico
Eric G. Moreno-Juáreza, b, *, Andrea Jiménez-Marínc, Fernando Álvareza
a Universidad Nacional Autónoma de México, Instituto de Biología, Colección Nacional de Crustáceos, Tercer Circuito s/n, Ciudad Universitaria, Coyoacán, 04510 Ciudad de México, Mexico
b Universidad Nacional Autónoma de México, Posgrado en Ciencias Biológicas, Instituto de Biología, Colección Nacional de Crustáceos, Tercer Circuito s/n, Ciudad Universitaria, Coyoacán, 04510 Ciudad de México, Mexico
c Universidad Nacional Autónoma de México, Instituto de Biología, Laboratorio de Biología Molecular, Tercer Circuito s/n, Ciudad Universitaria, Coyoacán, 04510 Ciudad de México, Mexico
*Corresponding author: ericgmorenoj@gmail.com (E.G. Moreno-Juárez)
Received: 13 August 2025; accepted: 01 December 2025
Abstract
We report for the first time the complete mitochondrial genome of a crab in the family Trichodactylidae, that of the stygobitic Rodriguezia adani Álvarez and Villalobos, 2018. The mitogenome is 17,561 bp of length with a GC composition of 26.4% and comprises 13 protein coding genes (PCGs), 2 ribosomal subunits and 19 transfer RNA (tRNAs) genes; its ribosomal subunits are separated by 10 genes (5 PCGs and 19 tRNAs). Its phylogenetic position was obtained through Maximum Likelihood and Bayesian Inference analyses, both placed this species inside the subsection Heterotremata and as the sister group of the family Orithyiidae. Changes in the number of tRNAs could be the result of the adaptation to a stygobitic lifestyle. This is the first genomic resource for the Trichodactylidae and could be the initial step for future phylogenomic studies of this group.
Keywords: Stygobitic; Freshwater crab; Cave; Mitochondrion
Resumen
Reportamos el primer genoma mitocondrial completo de un cangrejo de la familia Trichodactylidae, el de la especie estigobítica Rodriguezia adani Álvarez y Villalobos, 2018. El mitogenoma tiene 17,561 pb de longitud, una composición de GC de 26.4% y contiene 13 genes codificantes de proteínas (PCGs), 2 subunidades ribosomales y 19 genes de RNA de transferencia (tRNAs); sus subunidades ribosomales están separadas por 10 genes (5 PCGs y 19 tRNAs). La posición filogenética obtenida a través de máxima verosimilitud e inferencia bayesiana ubica a esta especie dentro de la subsección Heterotremata y como grupo hermano de la familia Orithyiidae. Los cambios en el número de tRNAs podrían ser el resultado de la adaptación a un estilo de vida estigobítico. Este es el primer recurso genómico para los Trichodactylidae y posiblemente el paso inicial para futuros estudios filogenómicos de este grupo.
Palabras clave: Estigobítico; Cangrejo dulceacuícola; Cueva; Mitocondria
Introduction
The family Trichodactylidae H. Milne-Edwards, 1853, the single family in the superfamily Trichodactyloidea, is one of the 3 families of freshwater crabs in the American Continent (Álvarez et al., 2020). Rodriguezia Bott (1969) one of the 2 genera of Trichodactylidae found in Mexico; these are primary freshwater crabs distributed in southern Mexico (Álvarez & Villalobos, 2018; Magalhães & Türkay, 1996). The genus Rodriguezia comprises 3 species, 2 of them stygobitic; from them, Rodriguezia adani Álvarez & Villalobos, 2018 was the last one to be described (Fig. 1). Most of the research on this family has focused on its distribution, taxonomy, ecology, conservation and anatomy (Collins et al., 2009, 2011; Cumberlidge et al., 2014; Lima-Gomes et al., 2017; Magalhães et al., 2016; Magalhães & Türkay, 1996; Weihrauch et al., 2004; Williner & Collins, 2013). However, few attempts have been made to understand its phylogenetic relationships, except for few molecular analyses performed to solve species complex issues in the genera Avotrichodactylus Pretzmann, 1968, Trichodactylus Latreille, 1828 and Dilocarcinus Milne Edwards, 1853 (Caetano-França et al., 2024; Ojeda et al., 2013; Souza-Carvalho et al., 2017). Studies using genomic sequencing for this family are lacking, only recently a study on the genome size of Trichodactylus fluviatilis Latreille, 1828 was published (Barioto et al., 2024). To further advance our knowledge on the phylogeny and evolution of the Trichodactylidae, we present the first complete mitochondrial genome for the family.
Materials and methods
The organism used in this study was collected in the type locality, Aguas Blancas Cave, Tabasco, Mexico (17º36’22.06” N, 92º27’43.63” W, Fig. 2) and deposited in the Colección Nacional de Crustáceos (CNCR), of the Instituto de Biología, Universidad Nacional Autónoma de México (IB-UNAM), with catalog number CNCR 36762 (https://www.ib.unam.mx/ib/colecciones-biologicas/colecciones-zoologicas, Dr. Fernando Álvarez (falvarez@ib.unam.mx)). The organism was collected under license N° SGPA/DGVS/03775/22, provided by Semarnat. Its taxonomic identity was corroborated with Álvarez and Villalobos (2018) publication.
The DNA was purified from muscle tissue of the fifth pereopod with the Animal and Fungi DNA preparation kit, Jena Bioscience. Quality and concentration of DNA were determined with a NanoDrop 2000 spectrophotometer and Qubit 4 Fluorometer, respectively. The library used was prepared with Illumina DNA Prep Kit (Illumina, Inc.), following the Trevisan et al. (2019) protocol. The sequencing was conducted in an Illumina NextSeq 500 sequencer, using a 300-cycle cartridge in a Paired End (PE) 2X150 cycles configuration at the Massive Sequencing and Bioinformatic Unit of the Instituto de Biotecnología, UNAM.
A total of 11,090,166 raw sequences were obtained, its quality was measured with FastQC v. 0.11.9 (Andrews, 2010), and low quality reads (Q < 28) and adapters were removed with Trimmomatic v. 0.39 (Bolger et al., 2014). SPAdes v 3.15,1 (Bankevich et al., 2012) was implemented as assembler on Galaxy (The Galaxy Community, 2022) with k-mer values of 33, 55, 77, 105. The final sequence assembled was analyzed with MITOS (Bernt et al., 2013) to obtain the gene order and annotation. The framework of the Protein Coding Genes (PCGs) was corroborated with Geneious v. 2024.4 (Biomatters Inc., Auckland, New Zealand). To discard any issue during the assembly we performed the protocol of Vera-Paz et al. (2022). The depth average coverage was obtained with the online protocol of Ni et al. (2023). The final gene map was obtained with Chloroplot (Zheng et al., 2020).
To corroborate the phylogenetic position of R. adani, we initially based our selection of taxa on Tsang et al. (2014) and Wolfe et al. (2023), whose partial sequence-based phylogenies recovered Trichodactylidae together with Orithyiidae, Chasmocarcinidae, and Bellidae as a sister group to all Heterotremata. However, the only available mitogenome from that group was Orythia sinica (Orithyiidae), so to give a general idea of the phylogenetic position of R. adani,we selected other available mitogenomes from families and superfamilies representative of Heterotremata, species belonging to primary families of freshwater crabs, species of Thoracotremata, and Ranina ranina (Podotremata) as an outgroup (Table 1).
Table 1
Species included in the phylogenetic analysis and GenBank accession numbers.
| Species | Accession number | Reference |
| Rodriguezia adani | PQ064124 | This study |
| Ranina ranina | AB752308 | Unpublished |
| Tzotzilthelphusa villarosalensis | OP295767 | Moreno-Juárez et al., 2023 |
| Longpotamon yangtsekiens | KY785879 | Yuhui et al., 2017 |
| Ocypode ceratophthalmus | LN611669 | Tan et al., 2014 |
| Eriocheir japonica | FJ455505 | Wang et al., 2016 |
| Pachygrapsus crassipes | KC878511 | Yu et al., 2014 |
| Orithyia sinica | MG840649 | Zhong et al., 2018 |
| Chionoecetes japonicus | MT750295 | Kim et al., 2020 |
| Maguimithrax spinosissimus | KM405516 | Márquez et al., 2016 |
| Maja crispata | KY650651 | Basso et al., 2017 |
| Maja squinado | KY650652 | Basso et al., 2017 |
| Segonzacia mesatlantica | KY541839 | Mandon et al., 2017 |
| Austinograea alayseae | KC851803 | Kim et al., 2014 |
| Gandalfus puia | KR002727 | Kim et al., 2016 |
| Echinoecus nipponicus | MG574831 | Lee et al., 2018 |
| Pilumnus vespertilio | MF457402 | Tan et al., 2018 |
| Atergatis floridus | MG792341 | Karagozlu, Barbon et al., 2018 |
| Etisus anaglyptus | MG751773 | Karagozlu, Dihn et al., 2018 |
| Epixanthus frontalis | MF457404 | Tan et al., 2018 |
| Leptodius sanguineus | KT896744 | Sung et al., 2016 |
| Myomenippe fornasiniiq | LK391943 | Tan et al., 2016a |
| Myra affinis | MW192449 | Zhang et al., 2022 |
| Pyrhila pisum | KU343210 | Park et al., 2017 |
| Ashtoret lunaris | LK391941 | Tan et al., 2016b |
| Matuta victor | MT416712 | Huang et al., 2021 |
| Calappa bilineata | MN562587 | Lu et al., 2020 |
| Chaceon granulatus | AB769383 | Zhang et al., 2020 |
| Ovalipes punctatus | MH802052 | Unpublished |
| Scylla olivacea | FJ827760 | Unpublished |
| Charybdis bimaculata | MG787408 | Liu et al., 2018 |
| Callinectes sapidus | AY363392 | Place et al., 2005 |
| Portunus sanguinolentus | KT438509 | Ma et al., 2016 |
Table 2
Best partition scheme and model selection resulting from the analyses on IQ-Tree.
| Partition | Nucleotide substitution model | Reference |
| 12S | TVM + F + G4 | |
| 16S | TVM + F + I + G4 | |
| ATP6 pos1, COX2 pos1, COX3 pos1, CYTB pos1, ND3 pos1 | GTR + F + I + G4 | Tavaré, 1986 |
| ATP6 pos2, CYTB pos2, ND3 pos2 | GTR+F+I+G4 | Tavaré, 1986 |
| ATP6 pos3, ATP8 pos3, COX1 pos3, COX2 pos3, COX3 pos3, CYTB pos3, ND3 pos3 | GTR+F+I+G4 | Tavaré, 1986 |
| ATP8 pos1, ND2 pos1, ND6 pos1 | GTR+F+I+G4 | Tavaré, 1986 |
| ATP8 pos2, ND2 pos2, ND6 pos2 | GTR+F+I+G4 | Tavaré, 1986 |
| COX1 pos1 | TIM2+F+I+G4 | |
| COX1 pos2, COX2 pos2, COX3 pos2 | TVM+F+I+G4 | |
| ND1pos1, ND4 pos1, ND4L pos1, ND5 pos1 | GTR+F+I+G4 | Tavaré, 1986 |
| ND1 pos2, ND4 pos2, ND4L pos2, ND5 pos2 | GTR+F+I+G4 | Tavaré, 1986 |
| ND1 pos3, ND4 pos3, ND4L pos3, ND5 pos3 | TN+F+I+G4 | Tamura and Nei, 1993 |
| ND2 pos3, ND6 pos | TN+F+G4 | Tamura and Nei, 1993 |
A total of 15 mitochondrial genes (13 PCGs and 2 rRNA) were individually aligned with Mafft v. 7 online service (Katoh et al., 2019). The final concatenated matrix was analyzed with a codon partition merging and a model selection analysis, implemented on IQ-tree (Chernomor et al., 2016; Kalyaanamoorthy et al., 2017), resulting in 13 partitions and nucleotide substitution models (Table 2). Two phylogenetic inference methods were implemented, the maximum likelihood (ML) analysis was performed in IQ-Tree with 10,000 ultrafast bootstrap analysis (Hoang et al., 2018; Trifinopoulos et al., 2016). The Bayesian Inference (BI) analysis was performed with Exabayes (Aberer et al., 2014) with 20 million generations, sampling every 10,000 generations, standard deviation of split frequencies convergence value of 0.01 and 25% of burn-in.
Results
The complete mitochondrial genome of R. adani (GenBank: PQ064124; associated BioProject, SRA, and Bio-Sample numbers are PRJNA1139182, SRR29931217, and SAMN42764363, respectively) was obtained in only 1 contig with a length of 17,561 bp, an average depth of 125.8X and a GC composition of 26.4% (Fig. 3). It comprised 13 PCGs, 2 ribosomal RNA (rRNA) genes and 19 confirmed transfer RNA (tRNA) genes (Fig. 4, Table 3). Twenty-three genes are in the antisense strand: 9 PCGs (COX1, COX2, COX3, CYTB, ATP6, ATP8, ND1, ND3, ND6), and 14 tRNAs (tRNA-L1, K, D, G, A, R, N, S1, E, T, I, S2, M, W); and 11 are in the sense strand, 4 PCGs (ND1, ND4, ND4L, ND5), both rRNA genes (12S and 16S) and 5 tRNAs (tRNA-P, H, Q, Y, V); 1 tRNA-C is missing and tRNA-L2 and F are not confirmed. PCGs starting codons were ATG (COX1, COX2, COX3, ATP6, CYTB, ND2, ND4, ND4L), ATT (ATP8, ND5, ND6), ATC (ND3) and ATA (ND1). Most of the PCGs terminate with TAA, except for ND4 (TAG). Both phylogenetic analyses (ML, BI) recovered R. adani as the sister group of the family Orithyiidae with a high branch support (92/1) (Fig. 5).
Discussion
The family Trichodactylidae has been poorly studied molecularly and genomic sequencing of its species is non-existent, so this study contributes with the first mitochondrial genome sequenced from a stygobitic species. The gene order and topology found in R. adani is quite different from other crab mitochondrial genomes reported, this is due to the ribosomal subunits that are separated by several PCGs (5) and tRNAs (5). According to the mitochondrial patterns reported by Tan et al. (2019) this gene arrangement is not found in any other crab so far reported. Most decapod mitochondrial genomes present ribosomal subunits one next to the other or separated by tRNA-V or/and tRNA-Q, few decapod species (e.g., the crayfish Parastacus brasiliensis and Engaeus quadrimanus, reported in Tan et al., 2019) present ribosomal subunits separated by PCGs like R. adani. With respect to the tRNAs, although in mitochondrial genomes the most common number is 22, R. adani just presents 19 confirmed; several species could present more or less tRNAs, depending on their evolutionary history (Romanova et al., 2016, 2020, 2021; Tan et al., 2019). In the case of R. adani, its stygobitic condition could be related to physiological adaptations that enable survival in low food availability conditions and low oxygen concentrations (Hervant et al., 1999, 2001). It has been documented that in some instances metabolic changes can lead to the duplication or deletion of certain tRNAs, which can optimize the synthesis of enzymes or proteins that play an important role in these new metabolic processes (Romanova et al., 2021; Tan et al., 2019; Xing et al., 2025). Regarding tRNAs-L2 and F, both were recognized by MITOS and tRNAscan-SE but not supported by BlastN. It is possible that these tRNAs sequences are so novel that there is no sequence to compare them with, or an error may have occurred during assembly or annotation; for these reasons we decided to leave them as unconfirmed until other mitogenomes of the family are reported to corroborate or invalidate their presence through Romanova et al. (2016, 2020) protocol.
Table 3
Comparative table of the differences between R. adani and other brachyuran species.
| Organism | Size | Gene number | tRNAs | GC % composition | Reference |
| Rodriguezia adani | 17,561 | 34 | 19 | 26.4 | This study |
| Orithya sinica | 15,568 | 37 | 22 | 30.5 | Zhong et al., 2018 |
| Chionoecetes japonicus | 16,060 | 37 | 22 | 28.2 | Kim et al., 2020 |
| Callinectes sapidus | 16,263 | 37 | 22 | 30.9 | Place et al., 2005 |
| Eriocheir japonica | 16,352 | 37 | 22 | 28.4 | Wang et al., 2016 |
| Maja crispata | 16,592 | 37 | 22 | 29.7 | Basso et al., 2017 |
| Myra affinis | 15,349 | 37 | 22 | 29.4 | Basso et al., 2017 |
| Gandalfus puia | 15,548 | 37 | 22 | 30.1 | Kim et al., 2016 |
| Pilumnus vespertilio | 16,222 | 37 | 22 | 28.9 | Tan et al., 2018 |
| Epixanthus frontalis | 15,993 | 37 | 22 | 34.1 | Tan et al., 2018 |
| Matuta victor | 15,782 | 37 | 22 | 29.9 | Huang et al., 2021 |
| Calappa bilineata | 15,606 | 37 | 22 | 31.3 | Lu et al., 2020 |
| Ovalipes punctatus | 16,084 | 37 | 22 | 31.9 | Unpublished |
Regarding the phylogenetic position of R. adani, it was recovered as the sister group of the Orithyiidae, forming a clade that is the sister group to the rest of the subsection Heterotremata (Fig. 4).
Our results coincide with those of Wolfe et al. (2023), who using sequences of 10 genes, produced a phylogeny where the Orithyiidae and the Trichodactylidae are described as sister groups. Other coincidences with Wolfe et al. (2023) phylogenetic tree are the polyphyletic origin of primary freshwater crabs, Potamidae related to Thoracotremata, while Oregoniidae, Mithracidae, and Majidae are grouped in Majoidea and Portunidae, Ovalipidae and Geryonidae are grouped in Portunoidea. The phylogenetic relationships of the remaining species were not the aim of this work.
The low branch supports for these clades, likely due to a limited taxon sampling, preclude further interpretation. Future studies with more comprehensive sampling as in Tsang et al. (2014), Tan et al. (2019) or Wolfe et al. (2023), are needed to resolve these relationships with confidence (Nabhan & Sakar, 2012; Som, 2015).
Acknowledgements
We thank Ricardo Grande and Alejandro Sánchez for their assistance and advise during the genomic libraries’ construction and sequencing at the Unidad Universitaria de Secuenciación Masiva y Bioinformática, Instituto de Biotecnología, UNAM. This paper is part of the requirements for the Doctoral degree at Posgrado en Ciencias Biológicas, UNAM for EGMJ. EGMJ thanks Consejo Nacional de Humanidades, Ciencias y Tecnologías for the doctoral scholarship granted 2020-000013-01NACF-12928. Óscar Pérez Flores offered important advice during the phylogenetic analyses, which are greatly appreciated. Sandra Vera offered advice during the assembly and annotation which are greatly appreciated. José Luis Villalobos Hiriart, Kevin Madrigal and Josselyne Santillán for their help in the collection of the specimen; to the reviewers Ricardo Grande, Marco Solano and Carlos Pedraza for their interest in this work and their valuable comments. Finally, we thank Cristian Cervantes from the UniSSE, IB-UNAM. Funds were provided by Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica, Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México grant IV200122 awarded to FA.
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