Contrasting Modes of Mitochondrial Genome Evolution in Sister Taxa of Wood-Eating Marine Bivalves (Teredinidae and Xylophagaidae)

Author:

Li Yuanning1ORCID,Altamia Marvin A2ORCID,Shipway J Reuben3ORCID,Brugler Mercer R45ORCID,Bernardino Angelo Fraga6ORCID,de Brito Thaís Lima7ORCID,Lin Zhenjian8ORCID,da Silva Oliveira Francisca Andréa7ORCID,Sumida Paulo9ORCID,Smith Craig R10ORCID,Trindade-Silva Amaro7ORCID,Halanych Kenneth M11ORCID,Distel Daniel L2ORCID

Affiliation:

1. Institute of Marine Science and Technology, Shandong University , Qingdao 266237 , China

2. Ocean Genome Legacy Center, Department of Marine and Environmental Science, Northeastern University , Nahant, Massachusetts 01908 , USA

3. Marine Biology and Ecology Research Centre, School of Biological and Marine Sciences, University of Plymouth , Plymouth PL4 8AA , United Kingdom

4. Department of Natural Sciences, University of South Carolina Beaufort , 801 Carteret Street, Beaufort, South Carolina 29902 , USA

5. Division of Invertebrate Zoology, American Museum of Natural History , Central Park West at 79th Street, New York, New York 10024 , USA

6. Departamento de Oceanografia, Universidade Federal do Espirito Santo , Vitória-ES , Brazil

7. Drug Research and Development Center, Department of Physiology and Pharmacology, Federal University of Ceará , Ceará , Brazil

8. Department of Medicinal Chemistry, University of Utah , Salt Lake City, Utah , USA

9. Departamento de Oceanografia Biológica, Instituto Oceanográfico da Universidade de São Paulo , São Paulo, SP , Brazil

10. Department of Oceanography, University of Hawai’i at Mãnoa , Hawaii , USA

11. Center for Marine Science, University of North Carolina Wilmington , North Carolina , USA

Abstract

Abstract The bivalve families Teredinidae and Xylophagaidae include voracious consumers of wood in shallow-water and deep-water marine environments, respectively. The taxa are sister clades whose members consume wood as food with the aid of intracellular cellulolytic endosymbionts housed in their gills. This combination of adaptations is found in no other group of animals and was likely present in the common ancestor of both families. Despite these commonalities, the two families have followed dramatically different evolutionary paths with respect to anatomy, life history, and distribution. Here, we present 42 new mitochondrial genome sequences from Teredinidae and Xylophagaidae and show that distinct trajectories have also occurred in the evolution and organization of their mitochondrial genomes. Teredinidae display significantly greater rates of amino acid substitution but absolute conservation of protein-coding gene order, whereas Xylophagaidae display significantly less amino acid change but have undergone numerous and diverse changes in genome organization since their divergence from a common ancestor. As with many bivalves, these mitochondrial genomes encode 2 ribosomal RNAs, 12 protein-coding genes, and 22 tRNAs; atp8 was not detected. We further show that their phylogeny, as inferred from amino acid sequences of 12 concatenated mitochondrial protein-coding genes, is largely congruent with those inferred from their nuclear genomes based on 18S and 28S ribosomal RNA sequences. Our results provide a robust phylogenetic framework to explore the tempo and mode of mitochondrial genome evolution and offer directions for future phylogenetic and taxonomic studies of wood-boring bivalves.

Funder

Fogarty International Center of the National Institutes of Health

National Science Foundation

Gordon and Betty Moore Foundation

CNPq

CAPES

Publisher

Oxford University Press (OUP)

Subject

Genetics,Ecology, Evolution, Behavior and Systematics

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