The Antarctic Weddell seal genome reveals evidence of selection on cardiovascular phenotype and lipid handling

Hyun Ji Noh,S Anne Schulberg,Allyson G Hindle,Jeremy Johnson,Kaitlin N Allen,Michael L Fitzgerald,Luis A Hückstädt,Jason Turner-Maier,Jessica Alfoldi,Warren M Zapol,Emmanuel S Buys,Kerstin Lindblad-Toh,Daniel P Costa,Annabelle J Batten,Elinor K Karlsson

doi:10.1038/s42003-022-03089-2

Abstract

The Weddell seal (Leptonychotes weddellii) thrives in its extreme Antarctic environment. We generated the Weddell seal genome assembly and a high-quality annotation to investigate genome-wide evolutionary pressures that underlie its phenotype and to study genes implicated in hypoxia tolerance and a lipid-based metabolism. Genome-wide analyses included gene family expansion/contraction, positive selection, and diverged sequence (acceleration) compared to other placental mammals, identifying selection in coding and non-coding sequence in five pathways that may shape cardiovascular phenotype. Lipid metabolism as well as hypoxia genes contained more accelerated regions in the Weddell seal compared to genomic background. Top-significant genes were SUMO2 and EP300; both regulate hypoxia inducible factor signaling. Liver expression of four genes with the strongest acceleration signals differ between Weddell seals and a terrestrial mammal, sheep. We also report a high-density lipoprotein-like particle in Weddell seal serum not present in other mammals, including the shallow-diving harbor seal.

Highlights

The Weddell seal (Leptonychotes weddellii) thrives in its extreme Antarctic environment
We found that acceleration signals in the Weddell seal genome were significantly stronger in both gene lists compared to genome-wide Weddell seal accelerated regions (WedARs) (mean false discovery rate (FDR) of 557,489 genome-wide split elements = 0.661)
We found that lipid metabolism genes but not hypoxia signaling genes, showed stronger acceleration signals compared to the genome-wide data for these two pinnipeds

Summary

Introduction

The Weddell seal (Leptonychotes weddellii) thrives in its extreme Antarctic environment. Cell specializations that protect against low oxygen injury[13] are important for diving ability These are likely coupled with additional metabolic mechanisms that reduce energy expenditures during submergence[14,15,16]. Advances in genomics have rapidly expanded the number of whole genomes available for comparison across species[23], allowing the systematic interrogation and understanding of both protein and regulatory changes through evolutionary events[24,25,26] Such analyses may enable discovery of specific genetic strategies facilitating cell and animal survival at low oxygen pressures and the absence of cardiovascular diseases despite hyperlipidemia, which may have indications for human medicine. Despite clear phenotypic convergence among marine mammals (e.g., hydrodynamic body shapes and extended breath-holding abilities occurring in pinnipeds, cetaceans, and sirenians), analyses of molecular convergence have revealed only limited similarities among major proteins of interest[31,35,36,37]

Methods

Results

Conclusion