Sirenian genomes illuminate the evolution of fully aquatic species within the mammalian superorder afrotheria

• Published in: Nature communications 2024-07, Vol.15 (1), p.5568-19, Article 5568
• Main Authors: Tian, Ran, Zhang, Yaolei, Kang, Hui, Zhang, Fan, Jin, Zhihong, Wang, Jiahao, Zhang, Peijun, Zhou, Xuming, Lanyon, Janet M., Sneath, Helen L., Woolford, Lucy, Fan, Guangyi, Li, Songhai, Seim, Inge
• Format: Article
• Language: English
• Subjects: 13/1; 13/109; 13/44; 45/22; 45/23; 45/90; 45/91; 631/158/672; 631/181/2474; 631/208/182; Activity patterns; Adaptation; Amino acids; Animals; Appendages; Aquatic mammals; Aquatic organisms; Aquatic Organisms - genetics; Australia; Biological clocks; Biological Evolution; Circadian Clocks - genetics; Circadian rhythm; Circadian rhythms; CLOCK protein; Evolution, Molecular; Genetic diversity; Genome - genetics; Genomes; Humanities and Social Sciences; Iodides; Iodine; Mammals - genetics; Marine mammals; multidisciplinary; Period 2 protein; Phylogeny; Population genetics; Protein transport; Science; Science (multidisciplinary)
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-49769-x

Sirenians of the superorder Afrotheria were the first mammals to transition from land to water and are the only herbivorous marine mammals. Here, we generated a chromosome-level dugong ( Dugong dugon ) genome. A comparison of our assembly with other afrotherian genomes reveals possible molecular adaptations to aquatic life by sirenians, including a shift in daily activity patterns (circadian clock) and tolerance to a high-iodine plant diet mediated through changes in the iodide transporter NIS ( SLC5A5 ) and its co-transporters. Functional in vitro assays confirm that sirenian amino acid substitutions alter the properties of the circadian clock protein PER2 and NIS. Sirenians show evidence of convergent regression of integumentary system (skin and its appendages) genes with cetaceans. Our analysis also uncovers gene losses that may be maladaptive in a modern environment, including a candidate gene ( KCNK18 ) for sirenian cold stress syndrome likely lost during their evolutionary shift in daily activity patterns. Genomes from nine Australian locations and the functionally extinct Okinawan population confirm and date a genetic break ~10.7 thousand years ago on the Australian east coast and provide evidence of an associated ecotype, and highlight the need for whole-genome resequencing data from dugong populations worldwide for conservation and genetic management. Sirenians are aquatic mammals that originated in Africa ~60 million years ago. Using comparative genomics of a new dugong genome, this study finds genetic adaptations shared by extant sirenians and assessed the diversity of dugongs in Australian waters and the functionally extinct Okinawan dugong.