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. 2014 Dec 12;3(1):27.
doi: 10.1186/2047-217X-3-27. eCollection 2014.

Two Antarctic penguin genomes reveal insights into their evolutionary history and molecular changes related to the Antarctic environment

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Free PMC article

Two Antarctic penguin genomes reveal insights into their evolutionary history and molecular changes related to the Antarctic environment

Cai Li et al. Gigascience. .
Free PMC article

Abstract

Background: Penguins are flightless aquatic birds widely distributed in the Southern Hemisphere. The distinctive morphological and physiological features of penguins allow them to live an aquatic life, and some of them have successfully adapted to the hostile environments in Antarctica. To study the phylogenetic and population history of penguins and the molecular basis of their adaptations to Antarctica, we sequenced the genomes of the two Antarctic dwelling penguin species, the Adélie penguin [Pygoscelis adeliae] and emperor penguin [Aptenodytes forsteri].

Results: Phylogenetic dating suggests that early penguins arose ~60 million years ago, coinciding with a period of global warming. Analysis of effective population sizes reveals that the two penguin species experienced population expansions from ~1 million years ago to ~100 thousand years ago, but responded differently to the climatic cooling of the last glacial period. Comparative genomic analyses with other available avian genomes identified molecular changes in genes related to epidermal structure, phototransduction, lipid metabolism, and forelimb morphology.

Conclusions: Our sequencing and initial analyses of the first two penguin genomes provide insights into the timing of penguin origin, fluctuations in effective population sizes of the two penguin species over the past 10 million years, and the potential associations between these biological patterns and global climate change. The molecular changes compared with other avian genomes reflect both shared and diverse adaptations of the two penguin species to the Antarctic environment.

Keywords: Adaptation; Antarctica; Avian genomics; Evolution; Penguins.

Figures

Figure 1
Figure 1
Phylogenetic relationships and changes in effective population sizes of two penguin species. (A) Phylogeny of two penguins and six closely related aquatic species (northern fulmar Fulmarus glacialis; great cormorant Phalacrocorax carbo; crested ibis Nipponia nippon; dalmatian pelican Pelecanus crispus; little egret Egretta garzetta; red-throated loon Gavia stellata) (blue names), and a land bird (zebra finch Taeniopygia guttata). The estimates of topology and divergence times are from our avian phylogenomic study [24]. Horizontal bars at each node represent 95% credibility intervals of estimated divergence times. Above the tree are the geological timescale and temperature changes over the past 65 million years, relative to the present [26]. PETM, Paleocene–Eocene Thermal Maximum. (B) Dynamic changes of effective population sizes (N e) of two penguins inferred by the pairwise sequentially Markovian coalescent (PSMC) method. The thick curves depict the estimated N e values of the two penguins, and the thin curves represent PSMC bootstrapping estimates. (C) Enlargement of the period from 100 KYA to 10 ka in panel (B). MIS 4, Marine Isotope Stage 4; LGM, last glacial maximum. Temperature change data are from [33].
Figure 2
Figure 2
Penguin-specific duplications of keratinocyte β-keratin genes. (A) Numbers of keratinocyte β-keratin genes in the two penguins and other birds. Error bars indicate standard deviations. P-values were calculated by phylogenetic ANOVA. (B) Phylogenetic cladogram of keratinocyte β-keratin genes of the Adélie penguin (PYGAD, in blue), emperor penguin (APTFO, in red), and five aquatic relatives (northern fulmar, FULGL; crested ibis, NIPNI; great cormorant, PHACA; little egret, EGRGA; dalmatian pelican, PELCR). Shading in the tree indicates putative penguin-specific gene duplication events.
Figure 3
Figure 3
Cases of positively selected sites and non-neutral penguin-specific amino acid changes. (A) Positively selected sites in emperor penguin CNGB1 protein sequence. Cytoplasmic and transmembrane regions are separated by the dashed lines. Blue shading represents the membrane-spanning helix, and the cAMP binding domain is shown in grey. The posterior probabilities were calculated using BEB method in CODEML. (B) Positively selected sites in the FASN protein in the Adélie lineage (green dots) and the ancestral lineage (blue dots). The molecular binding domains of FASN are shown in light red, whereas the major catalytic domains are shown in grey. From left to right, beta-ketoacyl synthase (KS), acyl and malonyl transferases (MAT), enoyl reductase (ER), beta-ketoacyl reductase (KR), and thioesterase (TE). The posterior probabilities were calculated using BEB method in CODEML. (C) Non-neutral penguin-specific amino acid changes in the EVC2 protein. One substitution site is located in the Pfam domain EVC_like (PF12297).

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