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Two Antarctic Penguin Genomes Reveal Insights Into Their Evolutionary History and Molecular Changes Related to The Edinburgh Research Explorer Two Antarctic penguin genomes reveal insights into their evolutionary history and molecular changes related to the Antarctic environment Citation for published version: Li, C, Zhang, Y, Li, J, Kong, L, Hu, H, Pan, H, Xu, L, Deng, Y, Li, Q, Jin, L, Yu, H, Chen, Y, Liu, B, Yang, L, Liu, S, Zhang, Y, Lang, Y, Xia, J, He, W, Shi, Q, Subramanian, S, Millar, CD, Meader, S, Rands, CM, Fujita, MK, Greenwold, MJ, Castoe, TA, Pollock, DD, Gu, W, Nam, K, Ellegren, H, Ho, SY, Burt, DW, Ponting, CP, Jarvis, ED, Gilbert, MTP, Yang, H, Wang, J, Lambert, DM, Wang, J & Zhang, G 2014, 'Two Antarctic penguin genomes reveal insights into their evolutionary history and molecular changes related to the Antarctic environment', GigaScience, vol. 3, no. 1, pp. 27. https://doi.org/10.1186/2047-217X-3-27 Digital Object Identifier (DOI): 10.1186/2047-217X-3-27 Link: Link to publication record in Edinburgh Research Explorer Document Version: Publisher's PDF, also known as Version of record Published In: GigaScience Publisher Rights Statement: © 2014 Li et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. General rights Copyright for the publications made accessible via the Edinburgh Research Explorer is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The University of Edinburgh has made every reasonable effort to ensure that Edinburgh Research Explorer content complies with UK legislation. If you believe that the public display of this file breaches copyright please contact [email protected] providing details, and we will remove access to the work immediately and investigate your claim. Download date: 30. Sep. 2021 Li et al. GigaScience 2014, 3:27 http://www.gigasciencejournal.com/content/3/1/27 RESEARCH Open Access Two Antarctic penguin genomes reveal insights into their evolutionary history and molecular changes related to the Antarctic environment Cai Li1,2†,YongZhang1†,JianwenLi1†, Lesheng Kong3†,HaofuHu1,HailinPan1,LuohaoXu1,YuanDeng1,QiyeLi1,2, Lijun Jin1, Hao Yu1, Yan Chen1,BinghangLiu1, Linfeng Yang1, Shiping Liu1, Yan Zhang1, Yongshan Lang1, Jinquan Xia1,WeimingHe1, Qiong Shi1, Sankar Subramanian4, Craig D Millar5, Stephen Meader3, Chris M Rands3, Matthew K Fujita3,20,MatthewJGreenwold6,ToddACastoe7,8,DavidDPollock7,WanjunGu9, Kiwoong Nam10,21, Hans Ellegren10, Simon YW Ho11,DavidWBurt12, Chris P Ponting3,ErichDJarvis13, M Thomas P Gilbert2,14, Huanming Yang1,15,JianWang1, David M Lambert4*, Jun Wang1,15,16,17,18* and Guojie Zhang1,19* 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: Penguins, Avian genomics, Evolution, Adaptation, Antarctica Background like wings in wing-propelled diving or underwater flight Sphenisciformes (penguins), an avian order comprising [2]. To be competent for an underwater life, penguins six extant genera and 18 species [1], are flightless aquatic have undergone multiple morphological adaptations. For birds widely distributed in the Southern Hemisphere. instance, penguins have developed densely packed, scale- Although all extant penguins have completely lost the like feathers which are good for waterproof and thermal capacity for aerial flight, they employ modified flipper- insulation [3,4]; their eye lens and visual sensitivity of penguins are adapted for the efficiency of underwater predation [5-7]; to overcome buoyancy force in water, * Correspondence: [email protected]; [email protected]; [email protected] penguins have developed dense bones [8] and stiff wing †Equal contributors joints [9], and reduced the distal wing musculature 4 Environmental Futures Centre, Griffith University, Nathan QLD 4111, Australia [9,10]. 1China National GeneBank, BGI-Shenzhen, Shenzhen 518083, China Full list of author information is available at the end of the article © 2014 Li et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Li et al. GigaScience 2014, 3:27 Page 2 of 15 http://www.gigasciencejournal.com/content/3/1/27 Penguins are the most common birds in Antarctica. (Table 1), respectively. We annotated 598 and 627 non- Among 18 extant penguin species, eight (emperor (Apte- coding RNAs (ncRNA) in Adélie and emperor genomes, of nodytes forsteri), king (A. patagonicus), Adélie (Pygoscelis which 172 (Adélie) and 180 (emperor) were microRNAs adeliae), chinstrap (P. antarctica), gentoo (P. papua), (miRNAs). 6.47% (Adélie) and 7.38% (emperor) in the two macaroni (Eudyptes chrysolophus), royal (E. chrysolophus) assemblies are predicted to be repetitive elements (Table 1; and rockhopper (E. chrysocome)) live in the Antarctic Additional file 3: Table S2). However, the proportions of and sub-Antarctic areas, and two of them (Adélie and repetitive elements in the penguin genomes should be lar- emperor) make the Antarctic continent as their major ger, because the unassembled regions tend to contain many habitats [11,12]. Antarctica is one of the most hostile repetitive elements. By mapping the reads of short insert environments on earth. The penguins living in Antarctica size libraries to the genome assembly of each penguin, are subject to extremely low temperatures, high winds, we identified 2,559,440 and 3,410,305 heterozygous sites in and profound seasonal changes in the length of daylight emperor and Adélie, respectively. We obtained 8295 1:1 [13]. To live in such a harsh environment, penguins have orthologs of 48 birds (including Adélie and emperor pen- developed a complicated system in the head, wing, and guins) from the avian phylogenomics project [23,24], and legs for enhanced thermoregulation [14,15], and an effect- the CDS alignments of these orthologs were used to analyze ive management of energy storage for long-term fasting the ratio of nonsynonymous substitution rate to synonym- [16-18]. Because of their important roles in the Antarctic ous substitution rate (dN/dS) in penguin lineages. ecosystem and their sensitive responses to changes in marine and Antarctic climate, penguins are also among Analyses the widely studied organisms in climate change research Phylogenetic relationships of two penguins and closely [19-22]. related aquatic species The unique morphology and remarkable life histories In the avian phylogenomics study [24], we produced a of penguins have attracted broad interest from scientists highly resolved phylogenetic tree of 48 avian species as well as the general public. However, most previous representing almost all extant avian orders with whole- studies focused on ecological, physiological, behavioral, genome phylogenetic signals. The two penguins are in a or phylogenetic aspects of their biology, whereas the relatively basal position within a clade of aquatic birds molecular genetic bases of penguin adaptations remain (Figure 1A). Molecular dating of 48 birds was performed in largely unknown. As part of the avian phylogenomics the main companion study [24] using 19 fossil calibrations, project [23,24], we sequenced the genomes of two Ant- including the earlier Waimanu penguin
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