Positive selection over the mitochondrial genome and its role in the diversification of gentoo penguins in response to adaptation in isolation

• Published in: Scientific Reports
• Main Authors: Noll, D., Leon, F., Brandt, D., Pistorius, P., Le Bohec, Céline, Bonadonna, F., Trathan P., N., Barbosa, A., Raya Rey, A., Dantas G. P., M., Bowie R. C., K., Poulin, E., Vianna J., A.
• Other Authors: Pontificia Universidad Católica de Chile (UC), University of California Berkeley (UC Berkeley), University of California (UC), DST/NRF Centre of Excellence at the Percy FitzPatrick Institute for African Ornithology South Africa, Nelson Mandela University Port Elizabeth, Département Ecologie, Physiologie et Ethologie (DEPE-IPHC), Institut Pluridisciplinaire Hubert Curien (IPHC), Université de Strasbourg (UNISTRA)-Institut National de Physique Nucléaire et de Physique des Particules du CNRS (IN2P3)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Institut National de Physique Nucléaire et de Physique des Particules du CNRS (IN2P3)-Centre National de la Recherche Scientifique (CNRS), Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Université Paul-Valéry - Montpellier 3 (UPVM)-École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD France-Sud )-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro Montpellier, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Université de Montpellier (UM), British Antarctic Survey (BAS), Natural Environment Research Council (NERC), Museo Nacional de Ciencias Naturales Madrid (MNCN), Consejo Superior de Investigaciones Científicas Madrid (CSIC), Consejo Nacional de Investigaciones Científicas y Técnicas Buenos Aires (CONICET), Pontifícia Universidade Católica de Minas Gerais (PUC Minas), Universidad de Chile = University of Chile Santiago (UCHILE)
• Format: Article in Journal/Newspaper
• Language: English
• Published: HAL CCSD 2022
• Subjects: [SDV]Life Sciences [q-bio]; Antarctic; Southern Ocean; The Antarctic; Antarc*; Antarctica; Gentoo penguin; Pygoscelis papua
• Online Access: https://hal.science/hal-03618085; https://hal.science/hal-03618085/document; https://hal.science/hal-03618085/file/s41598-022-07562-0.pdf; https://doi.org/10.1038/s41598-022-07562-0

International audience Although mitochondrial DNA has been widely used in phylogeography, evidence has emerged that factors such as climate, food availability, and environmental pressures that produce high levels of stress can exert a strong influence on mitochondrial genomes, to the point of promoting the persistence of certain genotypes in order to compensate for the metabolic requirements of the local environment. As recently discovered, the gentoo penguins (Pygoscelis papua) comprise four highly divergent lineages across their distribution spanning the Antarctic and sub-Antarctic regions. Gentoo penguins therefore represent a suitable animal model to study adaptive processes across divergent environments. Based on 62 mitogenomes that we obtained from nine locations spanning all four gentoo penguin lineages, we demonstrated lineage-specific nucleotide substitutions for various genes, but only lineage-specific amino acid replacements for the ND1 and ND5 protein-coding genes. Purifying selection (dN/dS < 1) is the main driving force in the protein-coding genes that shape the diversity of mitogenomes in gentoo penguins. Positive selection (dN/dS > 1) was mostly present in codons of the Complex I (NADH genes), supported by two different codon-based methods at the ND1 and ND4 in the most divergent lineages, the eastern gentoo penguin from Crozet and Marion Islands and the southern gentoo penguin from Antarctica respectively. Additionally, ND5 and ATP6 were under selection in the branches of the phylogeny involving all gentoo penguins except the eastern lineage. Our study suggests that local adaptation of gentoo penguins has emerged as a response to environmental variability promoting the fixation of mitochondrial haplotypes in a non-random manner. Mitogenome adaptation is thus likely to have been associated with gentoo penguin diversification across the Southern Ocean and to have promoted their survival in extreme