Phylomitogenomics elucidates the evolution of symbiosis in Thoracotremata (Decapoda: Cryptochiridae, Pinnotheridae, Varunidae)
Background Thoracotremata belong to the large group of “true” crabs (infraorder Brachyura), and they exhibit a wide range of physiological and morphological adaptations to living in terrestrial, freshwater and marine habitats. Moreover, the clade comprises various symbiotic taxa (Aphanodactylidae, C...
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PeerJ Inc.
2023-10-01
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| Online Access: | https://peerj.com/articles/16217.pdf |
| _version_ | 1827608138692427776 |
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| author | Tao Xu Henrique Bravo Sancia E.T. van der Meij |
| author_facet | Tao Xu Henrique Bravo Sancia E.T. van der Meij |
| author_sort | Tao Xu |
| collection | DOAJ |
| description | Background Thoracotremata belong to the large group of “true” crabs (infraorder Brachyura), and they exhibit a wide range of physiological and morphological adaptations to living in terrestrial, freshwater and marine habitats. Moreover, the clade comprises various symbiotic taxa (Aphanodactylidae, Cryptochiridae, Pinnotheridae, some Varunidae) that are specialised in living with invertebrate hosts, but the evolutionary history of these symbiotic crabs is still partially unresolved. Methods Here we assembled and characterised the complete mitochondrial genomes (hereafter mitogenomes) of three gall crab species (Cryptochiridae): Kroppcarcinus siderastreicola, Opecarcinus hypostegus and Troglocarcinus corallicola. A phylogenetic tree of the Thoracotremata was reconstructed using 13 protein-coding genes and two ribosomal RNA genes retrieved from three new gall crab mitogenomes and a further 72 available thoracotreme mitogenomes. Furthermore, we applied a comparative analysis to characterise mitochondrial gene order arrangement, and performed a selection analysis to test for selective pressure of the protein-coding genes in symbiotic Cryptochiridae, Pinnotheridae, and Varunidae (Asthenognathus inaequipes and Tritodynamia horvathi). Results The results of the phylogenetic reconstruction confirm the monophyly of Cryptochiridae, which clustered separately from the Pinnotheridae. The latter clustered at the base of the tree with robust branch values. The symbiotic varunids A. inaequipes and T. horvathi clustered together in a clade with free-living Varunidae species, highlighting that symbiosis in the Thoracotremata evolved independently on multiple occasions. Different gene orders were detected in symbionts and free-living species when compared with the ancestral brachyuran gene order. Lastly, the selective pressure analysis detected two positively selected sites in the nad6 gene of Cryptochiridae, but the evidence for positive selection in Pinnotheridae and A. inaequipes and T. horvathi was weak. Adaptive evolution of mitochondrial protein-coding genes is perhaps related to the presumably higher energetic demands of a symbiotic lifestyle. |
| first_indexed | 2024-03-09T07:05:36Z |
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| id | doaj.art-de64f5ad5d564c048cbf9302f54a5540 |
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| language | English |
| last_indexed | 2024-03-09T07:05:36Z |
| publishDate | 2023-10-01 |
| publisher | PeerJ Inc. |
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| spelling | doaj.art-de64f5ad5d564c048cbf9302f54a55402023-12-03T09:39:54ZengPeerJ Inc.PeerJ2167-83592023-10-0111e1621710.7717/peerj.16217Phylomitogenomics elucidates the evolution of symbiosis in Thoracotremata (Decapoda: Cryptochiridae, Pinnotheridae, Varunidae)Tao Xu0Henrique Bravo1Sancia E.T. van der Meij2Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, NetherlandsGroningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, NetherlandsGroningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, NetherlandsBackground Thoracotremata belong to the large group of “true” crabs (infraorder Brachyura), and they exhibit a wide range of physiological and morphological adaptations to living in terrestrial, freshwater and marine habitats. Moreover, the clade comprises various symbiotic taxa (Aphanodactylidae, Cryptochiridae, Pinnotheridae, some Varunidae) that are specialised in living with invertebrate hosts, but the evolutionary history of these symbiotic crabs is still partially unresolved. Methods Here we assembled and characterised the complete mitochondrial genomes (hereafter mitogenomes) of three gall crab species (Cryptochiridae): Kroppcarcinus siderastreicola, Opecarcinus hypostegus and Troglocarcinus corallicola. A phylogenetic tree of the Thoracotremata was reconstructed using 13 protein-coding genes and two ribosomal RNA genes retrieved from three new gall crab mitogenomes and a further 72 available thoracotreme mitogenomes. Furthermore, we applied a comparative analysis to characterise mitochondrial gene order arrangement, and performed a selection analysis to test for selective pressure of the protein-coding genes in symbiotic Cryptochiridae, Pinnotheridae, and Varunidae (Asthenognathus inaequipes and Tritodynamia horvathi). Results The results of the phylogenetic reconstruction confirm the monophyly of Cryptochiridae, which clustered separately from the Pinnotheridae. The latter clustered at the base of the tree with robust branch values. The symbiotic varunids A. inaequipes and T. horvathi clustered together in a clade with free-living Varunidae species, highlighting that symbiosis in the Thoracotremata evolved independently on multiple occasions. Different gene orders were detected in symbionts and free-living species when compared with the ancestral brachyuran gene order. Lastly, the selective pressure analysis detected two positively selected sites in the nad6 gene of Cryptochiridae, but the evidence for positive selection in Pinnotheridae and A. inaequipes and T. horvathi was weak. Adaptive evolution of mitochondrial protein-coding genes is perhaps related to the presumably higher energetic demands of a symbiotic lifestyle.https://peerj.com/articles/16217.pdfAdaptive evolutionGall crabGene rearrangementMitogenomeSymbiosisPea crab |
| spellingShingle | Tao Xu Henrique Bravo Sancia E.T. van der Meij Phylomitogenomics elucidates the evolution of symbiosis in Thoracotremata (Decapoda: Cryptochiridae, Pinnotheridae, Varunidae) PeerJ Adaptive evolution Gall crab Gene rearrangement Mitogenome Symbiosis Pea crab |
| title | Phylomitogenomics elucidates the evolution of symbiosis in Thoracotremata (Decapoda: Cryptochiridae, Pinnotheridae, Varunidae) |
| title_full | Phylomitogenomics elucidates the evolution of symbiosis in Thoracotremata (Decapoda: Cryptochiridae, Pinnotheridae, Varunidae) |
| title_fullStr | Phylomitogenomics elucidates the evolution of symbiosis in Thoracotremata (Decapoda: Cryptochiridae, Pinnotheridae, Varunidae) |
| title_full_unstemmed | Phylomitogenomics elucidates the evolution of symbiosis in Thoracotremata (Decapoda: Cryptochiridae, Pinnotheridae, Varunidae) |
| title_short | Phylomitogenomics elucidates the evolution of symbiosis in Thoracotremata (Decapoda: Cryptochiridae, Pinnotheridae, Varunidae) |
| title_sort | phylomitogenomics elucidates the evolution of symbiosis in thoracotremata decapoda cryptochiridae pinnotheridae varunidae |
| topic | Adaptive evolution Gall crab Gene rearrangement Mitogenome Symbiosis Pea crab |
| url | https://peerj.com/articles/16217.pdf |
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