Selection-driven adaptation to the extreme Antarctic environment in the Emperor penguin

Abstract

The eco-evolutionary history of penguins is characterised by shifting from temperate to cold environments. Breeding in Antarctica, the Emperor penguin appears as an extreme outcome of this process, with unique features related to insulation, heat production and energy management. However, whether this species actually diverged from a less cold-adapted ancestor, more ecologically similar to its sister species, the King penguin, is still an open question. As the Antarctic colonisation likely resulted in vast changes in selective pressure experienced by the Emperor penguin, the relative quantification of the genomic signatures of selection, unique to each sister species, could answer this question. Applying phylogeny-based selection tests on 7651 orthologous genes, we identified a more pervasive selection shift in the Emperor penguin than in the King penguin, supporting the hypothesis that its extreme cold adaptation is a derived state. Furthermore, among candidate genes under selection, four (TRPM8, LEPR, CRB1, and SFI1) were identified before in other cold-adapted homeotherms, like the woolly Mammoth, while other 161 genes can be assigned to biological functions relevant to cold adaptation identified in previous studies. Location and structural effects of TRPM8 substitutions in Emperor and King penguin lineages support their functional role with putative divergent effects on thermal adaptation. We conclude that extreme cold adaptation in the Emperor penguin largely involved unique genetic options which, however, affect metabolic and physiological traits common to other cold-adapted homeotherms.

Fig. 1. Selection regime shifts in Emperor and King penguins genomes.

A Phylogenetic tree used in the selection tests based on Jarvis et al. and Pan et al. (refer to the original phylogenetic trees for nodes support). The Emperor and the King penguin are highlighted in blue and yellow, respectively. Note that branch length is not to scale. B Comparison between Emperor and King penguins for genes with FDR > 0.05 in each of the tests performed; bm: branch model; bsm: branch-site model; ω_i: ω in the target species; ω_b: background ω; For sake of completeness, we also show the genes putatively under selection according to RELAX (with K > 1). Inset. Venn diagram showing the overlap among CODEML (bm), aBSREL, and RELAX (K > 1). Note that the total number of genes is different between the Emperor and the King penguins and the size of the circles scales to the maximum in each of the two graphs. The overlap between CODEML (bm) or/and aBSREL with RELAX (K < 1) is 3, 1, and 1 gene, respectively (not shown).

Fig. 2. Ligand-free TRPM8 structure obtained by comparative modelling (four subunits in total, only two shown for clarity).

Carboxyl terminus domain, including the coiled coil, is shown in dark grey, while part of the rest of the protein is in light grey (MHR1/2/3 domains are not shown; see Supplementary Fig. S2 for completeness). Location of the substitutions found in Emperor (blue) and King (yellow) penguin lineages are also shown. H-score: hydrophobicity score (Monera et al. 1995); ΔΔG: free energy difference as estimated by FoldX (Schymkowitz et al. 2005).