Phylogenetic implications of mitogenome rearrangements in East Asian potamiscine freshwater crabs (Brachyura: Potamidae)
Graphical abstract
Introduction
The complete mitochondrial genome (mitogenome) of animals is characterized by its conserved gene content (37 genes) and by its condensed small genome size (14–18 kb). The first studies of mitogenomes focused mainly on vertebrates, and the arrangement and order of genes was considered to be widely conserved at the higher taxonomic levels (Boore and Brown, 1998). However, the increasing number of sequenced mitogenomes that are now becoming available suggests that gene order rearrangements have occurred frequently in some taxonomic groups: Ctenophora (Arafat et al., 2018), Mollusca (Guerra et al., 2018), and Anomura (Tan et al., 2018).
The highly diverse potamiscine freshwater crabs found in East Asia are fully adapted to a number of different freshwater habitats including major rivers, mountain streams, lakes, and wetlands, and many species are semi-terrestrial (Bott, 1970, Dai and Chen, 1985, Dai, 1999, Ng, 1988, Ng, 1987, Ng, 1985, Ng and Naiyanetr, 1993, Shih et al., 2009, Yeo and Ng, 2005, Yeo and Ng, 2009). In contrast to their marine relatives, primary freshwater crabs have a highly abbreviated life history (direct development, whereby hatchling crabs emerge from large eggs that develop in the female’s abdominal pouch), poor dispersal abilities, and complex burrowing behaviors (Cumberlidge, 1999, Dai, 1999). Recently, Next Generation Sequencing (NGS) has led the description of the complete mitogenomes of an increasing number of species of primary freshwater crabs and related decapods (Bai et al., 2018, Jia et al., 2018, Tan et al., 2018, Wang et al., 2016, Xing et al., 2017). The seven mitogenomes of primary freshwater crabs known to date (in four different potamiscine genera and the gecarcinucid genus Sommaniathelphusa) exhibit five different gene order rearrangements including one involving a protein-coding gene (Segawa and Aotsuka, 2005, Tan et al., 2018, Wang et al., 2016, Xing et al., 2017). The high mitogenome gene order rearrangement rate in freshwater crabs, together with the high species richness of potamiscine freshwater crabs, and the array of adaptations for life in freshwater, make this group an ideal candidate for evolutionary studies.
In addition, mitogenome gene order rearrangements can provide an independent dataset for studies of the evolutionary history of potamiscine crabs because it is unlikely that convergent evolution is responsible for the differences between taxa (Xing et al., 2017), given the relatively low mitogenome gene order rearrangement rate compared to the DNA nucleotide base substitution rate (Boore and Brown, 1998). In other words, shared mitogenome gene order rearrangement patterns in different taxonomic groups most likely provide evidence of common ancestry rather than being the product of convergent evolution (Basso et al., 2017, Tan et al., 2018).
In this study, we used NGS to make phylogenetic and comparative analyses of the mitochondrial gene order rearrangements based either on the complete sequence and/or the gene order. We also used the most comprehensive taxonomic sampling to date, extending the coverage of mitogenome data for primary freshwater crabs in East Asia from seven species and five genera to 56 species and 32 genera. We reconstructed ancestral states to determine the evolutionary processes that have produced the patterns of mitogenome gene order found in this study by applying three different analytic models, including TreeREx, Boundary-based Maximum Parsimony (BMP) analysis, and Event-based Maximum Parsimony (EMP) analysis. Our mitogenome gene order data include more than 60% of all Chinese and East Asian genera in the subfamily Potamiscinae. This broadened taxonomic sampling using an independent dataset to investigate species boundaries has enabled comparative studies of evolutionary diversification and of cryptic diversity. Here we highlight the importance of including mitogenomic gene order rearrangement studies to investigate the intrinsic diversity of freshwater crabs and other brachyurans.
Section snippets
Sample collection
A total of 13 species from 10 genera of potamiscines and one gecarcinucid species (Somanniathelphusa) were sampled for sequencing, including Huananpotamon lichuanense and Potamiscus motuoense that were re-sequenced using NGS (Table 1). In addition, mitogenomic gene order scanning based on NGS data were collected for 37 species belonging to 19 potamiscine genera (unpublished data). Our total taxon sampling of freshwater crabs for which we have mitogenome data was 56 species in 32 genera from two
Mitogenome features, gene duplication, and intergenic spaces
The novel mitogenome sequences were completely determined for 11 of the 13 species of potamiscines, and for one species of gecarcinucoid (Table 1). Two mitogenomes (Parapotamon spinescens and Tenuilapotamon latilum) were incomplete because of unconjugated gaps (two in the former, one in the latter) which meant that they could not be circularized unambiguously, although every gene was found within the 20,027 bp and 19,482 bp sequences, respectively (Table 1; Fig. 1). Of the newly sequenced
Discussion
In this study we used data from 19 mitogenome sequences, including 12 newly sequenced mitogenomes, to describe a total of ten unique mitogenome gene order patterns that are characteristic of freshwater crabs, all of which are different from the marine brachyuran ground pattern. Nine of the ten patterns are found in the 17 species of potamiscines, and all of them were successfully detected in 54 representative species belonging to 31 genera sampled across species of Potamiscinae from East Asia.
Acknowledgments
We are pleased to thank Associate Prof. Kai Jing (Yunnan Normal University), Prof. Xiaoping Yu (Shaanxi Normal University), Prof. Zhaohui Pan (Tibet Agriculture & Animal Husbandry University), Prof. Zhonghu Liu (Henan Agriculture University), Prof. Zuhao Huang (Jinggangshan University), Prof. Xiaoyong Chen, Dr. Kai He and Mr. Zhiwei Dong (Kunming Institute of Zoology, Chinese Academy of Sciences), Assosiate Prof. Dekui He (Institute of Hydrobiology, Chinese Academy of Sciences) and Xin Lu
References (76)
- et al.
The complete mitochondrial genome of Huananpotamon lichuanense (Decapoda: Brachyura) with phylogenetic implications for freshwater crabs
Gene
(2018) - et al.
The complete mitochondrial genome of the demosponge Negombata magnifica (Poecilosclerida)
Mol. Phylogenet. Evol.
(2008) - et al.
MITOS: Improved de novo metazoan mitochondrial genome annotation
Mol. Phylogenet. Evol.
(2013) - et al.
Big trees from little genomes: Mitochondrial gene order as a phylogenetic tool
Curr. Opin. Genet. Dev.
(1998) - et al.
A new genus and new species of freshwater crab (Decapoda: Brachyura: Potamidae Ortmann, 1896) from Yunnan Province, China
Zootaxa
(2017) - et al.
Freshwater crabs and the biodiversity crisis: Importance, threats, status, and conservation challenges
Biol. Conserv.
(2009) - et al.
More evolution underground: Accelerated mitochondrial substitution rate in Australian burrowing freshwater crayfishes (Decapoda: Parastacidae)
Mol. Phylogenet. Evol.
(2018) - et al.
Mitochondrial gene order evolution in Mollusca: Inference of the ancestral state from the mtDNA of Chaetopleura apiculata (Polyplacophora, Chaetopleuridae)
Mol. Phylogenet. Evol.
(2018) - et al.
Out of the Sichuan Basin: Rapid species diversification of the freshwater crabs in Sinopotamon (Decapoda: Brachyura: Potamidae) endemic to China
Mol. Phylogenet. Evol.
(2016) - et al.
The Australian fresh water isopod (Phreatoicidea: Isopoda) allows insights into the early mitogenomic evolution of isopods
Comp. Biochem. Physiol. - Part D Genomics Proteomics
(2010)
A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase
J. Mol. Biol.
The mitochondrial genome of the Japanese freshwater crab, Geothelphusa dehaani (Crustacea: Brachyura): Evidence for its evolution via gene duplication
Gene
Mitochondrial genome of the Chinese mitten crab Eriocheir japonica sinenesis (Brachyura: Thoracotremata: Grapsoidea) reveals a novel gene order and two target regions of gene rearrangements
Gene
ORDER within the chaos: Insights into phylogenetic relationships within the Anomura (Crustacea: Decapoda) from mitochondrial sequences and gene order rearrangements
Mol. Phylogenet. Evol.
Evolution of the tRNA gene family in mitochondrial genomes of five Meretrix clams (Bivalvia, Veneridae)
Gene
Complete mitochondrial DNA sequence of the swimming crab, Portunus trituberculatus (Crustacea: Decapoda: Brachyura)
Gene
Mitochondrial phylogenomics and genome rearrangements in the barklice (Insecta: Psocodea)
Mol. Phylogenet. Evol.
Insect mitochondrial control region: A review of its structure, evolution and usefulness in evolutionary studies
Biochem. Syst. Ecol.
Extensive mitochondrial gene rearrangements in Ctenophora: Insights from benthic Platyctenida
BMC Evol. Biol.
The highly rearranged mitochondrial genomes of the crabs Maja crispata and Maja squinado (Majidae) and gene order evolution in Brachyura
Sci. Rep.
An algorithm for inferring mitogenome rearrangements in a phylogenetic tree
Lect. Notes Comput. Sci. (including Subser. Lect. Notes Artif. Intell. Lect. Notes Bioinformatics) 5267
CREx: Inferring genomic rearrangements based on common intervals
Bioinformatics
Die Süßwasserkrabben von Europa, Asien, Australien-und ihre Stammgeschichte
Abh. Senckb. Naturforsch. Ges.
Duplication and remoulding of tRNA genes during the evolutionary rearrangement of mitochondrial genomes
Nature
A checklist for the classification and distribution of China’s freshwater crabs
Biodivers. Sci.
Sinopotamon baokangense sp. nov., a new freshwater crab with spoon-tipped cheliped fingers from Hubei Province, P.R. China (Decapoda, Brachyura, Potamidae)
Crustaceana
A new genus and species of primary freshwater crab and a new species of Artopotamon Dai & Chen, 1985 (Crustacea, Brachyura, Potamidae) from western Yunnan, China
Zootaxa
Designation of A Neotype for Freshwater Crab, Sinopotamon chengkuense Huang, Luo & Liu, 1986 (Decapoda:Brachyura:Potamidae)
Sichuan J. Zool.
Freshwater crabs of Xishuangbanna, Yunnan Province, China (Malacostraca:Crustacea: Parathelphusidae, Potamidae)
Acta Zootaxonomica Sin.
A preliminary report on the freshwater crabs of Hengduan Mountains area
Sinozoologia
Fauna Sinica. Crustacea: Decapoda: Parathelphusidae, Potamidae: 1-501, pis. 1-30
Mitochondrial genome evolution in species belonging to the Phialocephala fortinii s.l. - Acephala applanata species complex
BMC Genomics
Atp8 is in the ground pattern of flatworm mitochondrial genomes
BMC Genomics
TRDB - the tandem repeats database
Nucleic Acids Res.
The complete mitochondrial genome of Somanniathelphusa boyangensis and phylogenetic analysis of Genus Somanniathelphusa (Crustacea: Decapoda: Parathelphusidae)
PLoS ONE
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These authors contributed equally to this work.