Cyphoderia ampulla (Cyphoderiidae: Rhizaria), a tale of freshwater sailors: The causes and consequences of ecological transitions through the salinity barrier in a family of benthic protists

• Published in: Molecular ecology Vol. 31; no. 9; pp. 2644 - 2663
• Main Authors: González‐Miguéns, Rubén, Soler‐Zamora, Carmen, Useros, Fernando, Nogal‐Prata, Sandra, Berney, Cédric, Blanco‐Rotea, Andrés, Carrasco‐Braganza, María Isabel, Salvador‐Velasco, David, Guillén‐Oterino, Antonio, Tenorio‐Rodríguez, Daniel, Velázquez, David, Heger, Thierry J., Sanmartín, Isabel, Lara, Enrique
• Format: Journal Article
• Language: English
• Published: England Blackwell Publishing Ltd 01.05.2022; John Wiley and Sons Inc
• Subjects: adaptive morphology; Animals; Biodiversity; Cyphoderia; Cyphoderia ampulla; Cyphoderiidae; Cytochrome; Cytochromes; Deoxyribonucleic acid; DNA; Ecological effects; ecological transition; Ecosystem; Environmental DNA; Eukaryota; Eukaryotes; Fossils; Fresh Water; Gene sequencing; Humans; Military Personnel; Miocene; Mitochondria; Nucleotide sequence; Original; ORIGINAL ARTICLES; parallel evolution; Phylogeny; preadaptation; Rhizaria; rRNA; Sailors; Salinity; salinity barrier; Salinity effects; Sea level; Sediments; adaptive morphology; parallel evolution; ecological transition; preadaptation; salinity barrier; Cyphoderia
• ISSN: 0962-1083; 1365-294X
• DOI: 10.1111/mec.16424

The salinity barrier that separates marine and freshwater biomes is probably the most important division in biodiversity on Earth. Those organisms that successfully performed this transition had access to new ecosystems while undergoing changes in selective pressure, which often led to major shifts in diversification rates. While these transitions have been extensively investigated in animals, the tempo, mode, and outcome of crossing the salinity barrier have been scarcely studied in other eukaryotes. Here, we reconstructed the evolutionary history of the species complex Cyphoderia ampulla (Euglyphida: Cercozoa: Rhizaria) based on DNA sequences from the nuclear SSU rRNA gene and the mitochondrial cytochrome oxidase subunit I gene, obtained from publicly available environmental DNA data (GeneBank, EukBank) and isolated organisms. A tree calibrated with euglyphid fossils showed that four independent transitions towards freshwater systems occurred from the mid‐Miocene onwards, coincident with important fluctuations in sea level. Ancestral trait reconstructions indicated that the whole family Cyphoderiidae had a marine origin and suggest that ancestors of the freshwater forms were euryhaline and lived in environments with fluctuating salinity. Diversification rates did not show any obvious increase concomitant with ecological transitions, but morphometric analyses indicated that species increased in size and homogenized their morphology after colonizing the new environments. This suggests adaptation to changes in selective pressure exerted by life in freshwater sediments.