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

Abstract

Sirenians of the diverse superorder Afrotheria were the first mammals to retransition from land to water and are the sole herbivorous marine mammals, but little is known about the underlying genomic changes. Here, we generated a chromosome-level dugong (Dugong dugon) genome. A comparison of our assembly and a recent West Indian manatee genome with other afrotherian genomes revealed possible molecular solutions 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 confirmed 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, the only other fully aquatic mammal group. Our analysis also uncovered 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. Finally, genomes from nine Australian locations and the functionally extinct Okinawan population confirm and date a genetic break on the Australian east coast and highlight the need for whole-genome resequencing data from small or isolated dugong populations worldwide for conservation and genetic management.

The genome of African manatee Trichechus senegalensis reveals secondary adaptation to the aquatic environment

“…Meanwhile, a recent study confirmed that this gene is also inactivated in the West Indian manatee and dugong. 45 It has been proved that the nociceptive neurons in KCNK18 -KO mice showed a decreased threshold for activation and the skin nociceptive C-fibres showed an enhanced activation by cold. Consequently, the cold sensitivity of the KCNK18 -KO mice was enhanced.…”

“…Currently, the availability of resources for high-quality genome assembly in Afrotheria species remains limited, potentially obstructing the discovery of more nuanced evolutionary signatures within the Sirenia species. In the future, utilizing recently published high-quality dugong genomes, 45 , 48 we can delve deeper into the genetic basis of distinct adaptive evolutionary traits between manatees and dugongs, such as the tail fluke and skin morphology. Meanwhile, gene function verification experiments in vivo and in vitro should be further performed to validate the candidate genes we found in this study to be associated with the aquatic adaptive characteristics of the African manatee.…”