Phylomitogenomics elucidates the evolution of symbiosis in Thoracotremata (Decapoda: Cryptochiridae, Pinnotheridae, Varunidae)

Tao Xu; Henrique Bravo; Sancia E T van der Meij

doi:10.7717/peerj.16217

Phylomitogenomics elucidates the evolution of symbiosis in Thoracotremata (Decapoda: Cryptochiridae, Pinnotheridae, Varunidae)

PeerJ. 2023 Oct 16:11:e16217. doi: 10.7717/peerj.16217. eCollection 2023.

Authors

Tao Xu¹, Henrique Bravo¹, Sancia E T van der Meij^{1

2}

Affiliations

¹ Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, Netherlands.
² Marine Biodiversity Group, Naturalis Biodiversity Center, Leiden, Netherlands.

Abstract

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.

Keywords: Adaptive evolution; Gall crab; Gene rearrangement; Mitogenome; Pea crab; Symbiosis; Varunidae.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
Brachyura* / genetics
Gene Order
Genes, Mitochondrial
Phylogeny
Symbiosis / genetics

Grants and funding

Fieldwork by Henrique Bravo in Guadeloupe was funded by TREUB-maatschappij (Society for the Advancement of Research in the Tropics) and Flying Sharks. Fieldwork by Tao Xu in Curaçao was financed by Academy Ecology Fund Grant from the Royal Netherlands Academy of Arts and Sciences (No. KNAWWF/705/ECO202223). The scholarship of Tao Xu was provided by the China Scholarship Council (No. 201907565038). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.