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Dipartimento Di Biologia Transcriptomics and Population

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Dipartimento Di Biologia Transcriptomics and Population UNIVERSITÀ DEGLI STUDI DI PADOVA Dipartimento di Biologia Scuola di Dottorato di Ricerca in Bioscienze e Biotecnologie Indirizzo Biologia Evoluzionistica Ciclo XXVI Transcriptomics and population differentiation in two notothenioid Antarctic fish Trascrittomica e differenziamento di popolazione in due specie di pesci nototenioidei antartici Direttore della Scuola: Ch.mo Prof. Giuseppe Zanotti Coordinatore d’indirizzo: Ch.mo Prof. Andrea Pilastro Supervisore: Ch.mo Prof. Lorenzo Zane Dottoranda: Cecilia Agostini ! "! CONTENTS LIST OF ABBREVIATIONS 5 LIST OF PAPERS 7 ABSTRACT 9 GENERAL INTRODUCTION 11 AIMS OF THE THESIS 15 STUDY SPECIES 16 The Chionodraco genus 16 Pleuragramma antarcticum 18 PAPER EXTENDED ABSTRACTS 21 Paper I 21 Paper II 23 Paper III 24 Paper IV 24 Paper V 25 Paper VI 27 Paper VII 30 GENERAL CONCLUSIONS 32 PAPERS 35 Paper I 37 Paper II 39 Paper III 41 Paper IV 43 Paper V 45 Paper VI 47 Paper VII 49 RIASSUNTO 51 REFERENCES 53 ACKNOWLEDGEMENTS 63 ! #! ! $! LIST OF ABBREVIATIONS ABC = approximate Bayesian computation AFGP = antifreeze glycoprotein AP = Antarctic Peninsula ATP = adenosine triphosphate BLAST = basic local alignment search tool cDNA = complementary DNA DNA = deoxyribonucleic acid e.g. = exempli gratia EST = expressed sequence tag HSP = heat-shock protein HSR = heat-shock response HW = Hardy-Weinberg i.e. = Id est mRNA = messenger RNA mtDNA = mitochondrial DNA MYA = million years ago PCR = polymerase chain reaction PhD = Philosophiae Doctor RNA = ribonucleic acid SL = standard length TLP = trypsinogen-like protease ! %! ! &! LIST OF PAPERS This thesis is based on seven papers (three primer notes and four scientific articles), six of which have been published in scientific journals and one is under revision: I. Coppe A*, Agostini C*, Marino IAM, Zane L, Bargelloni L, Bortoluzzi S, Patarnello T (2013). Genome evolution in the cold: Antarctic icefish muscle transcriptome reveals selective duplications increasing mitochondrial function. Genome Biology and Evolution, 5(1): 45-60. DOI: 10.1093/gbe/evs108. *Equally contributing first authors II. Marino IAM, Agostini C, Papetti C, Bisol PM, Zane L, and Patarnello T. Isolation, characterization and multiplexing of expressed sequence tag-linked microsatellite loci for the Antarctic icefish Chionodraco hamatus. In: Molecular Ecology Resources Primer Development Consortium, Agostini C, Agudelo PA et al. (2011). Permanent Genetic Resources added to Molecular Ecology Resources Database 1 October 2010-30 November 2010. Molecular Ecology Resources, 11(2), 418-421. DOI: 10.1111/j.1755-0998.2010.02970.x III. Papetti C, Marino IAM, Agostini C, Bisol PM, Patarnello T, Zane L (2011). Characterization of novel microsatellite markers in the Antarctic silverfish Pleuragramma antarcticum and cross species amplification in other Notothenioidei. Conservation Genetics Resources, 3(2): 259-262. DOI: 10.1007/s12686-010-9336-9 IV. Agostini C, Marino IAM, Patarnello P, Zane L. Isolation, characterization and multiplexing of sixteen EST-linked microsatellite loci in the Antarctic silverfish Pleuragramma antarcticum. In: Molecular Ecology Resources Primer Development Consortium, Agostini C, Albaladejo RG et al. (2013). Permanent Genetic Resources added to Molecular Ecology Resources Database 1 April 2013- 31 May 2013. Molecular Ecology Resources 13, 966-968. DOI: 10.1111/1755- 0998.12140 V. Agostini C, Papetti C, Patarnello T, Mark FC, Zane L, Marino IAM (2013). Putative selected markers in the Chionodraco genus detected by interspecific outlier tests. Polar Biology, 36(10): 1509-1518. DOI: 10.1007/s00300-013-1370-0 VI. Marino IAM, Benazzo A, Agostini C, Mezzavilla M, Hoban SM, Patarnello T, Zane L, Bertorelle G (2013). Evidence for past and present hybridization in three Antarctic icefish species provides new perspectives on an evolutionary radiation. Molecular Ecology, 22(20): 5148-5161. DOI: 10.1111/mec.12458 VII. Agostini C, Patarnello T, Ashford J, Torres J, Zane L. Has climate change promoted genetic fragmentation in ice-dependent Pleuragramma antarcticum? Journal of Biogeography, under revision For Paper I, I was involved in the annotation of the transcriptome and in the process of identification of duplicated genes; I performed the enrichment analysis using David, I participated in the interpretation of results and I had the main responsibility for writing the ! '! paper. For Paper II, I was involved in primer isolation and I performed most of the experimental work. For Paper III, I performed the cross-species amplification of primers in the Chionodraco genus and I obtained descriptive statistics of cross-amplification. For Papers IV, V and VII, I had the main responsibility for experiments, analyses and for writing the paper. For Paper VI, I performed most of the experimental work and I was involved in part of the analyses (analysis of the genetic variability level and of the pattern of genetic differentiation using F-statistics and the program Structure). ! (! ABSTRACT Antarctic notothenioids radiated over past millions of years in extremely cold waters, they display a wide range of adaptations to withstand the cold and now dominate the Antarctic fish fauna. These fish may be extremely vulnerable to climate change with possible cascading effects on the entire Antarctic marine ecosystem. Therefore, crucial tasks are the concomitant study of the genomic basis of cold adaptation, the analysis of differentiation processes resulting from past and present climate change and a close survey of the current level of genetic variation and population structure. We considered four species of the Notothenioidei suborder: the three recently derived species of the Chionodraco genus, namely Chionodraco hamatus, Chionodraco rastrospinosus and Chionodraco myersi, and Pleuragramma antarcticum. The Chionodraco genus belongs to the family Channichthyidae (icefish), unique among vertebrates for the lack of hemoglobin and myoglobin expression in skeletal muscle. Oxygen delivery to tissues is ensured by a marked remodelling of the cardio-vascular system and by exceptionally high mitochondrial densities in the muscle. P. antarcticum (Nototheniidae) is the only notothenioid with a complete pelagic life cycle; it is dependent on sea ice and plays a key role in the trophic web of the Antarctic marine ecosystem. Analyses performed in this PhD can be grouped in two major lines of research: 1) the deepening of the knowledge on the genetic and genomic basis of icefish adaptation to the cold; 2) the analysis of patterns of intra- and inter-specific genetic differentiation with particular emphasis on how past and present environmental conditions have shaped and are influencing the fish genetic structure. With regard to the first line of research, we reconstructed and annotated the first normalized transcriptome of C. hamatus skeletal muscle and we exploited deep sequencing information of this energy-dependent tissue to test the hypothesis of duplication of genes involved in mitochondrial function. Using a dedicated bioinformatic pipeline we identified 124 duplicated genes specific to the icefish lineage. Significantly more duplicates were found in C. hamatus when transcriptome data were compared with whole genome data of model fish. Duplicated genes were significantly enriched in proteins with mitochondrial localization, involved in mitochondrial function and biogenesis. The combination of high mitochondrial densities and the maintenance of duplicated genes involved in mitochondrial function might confer a selective advantage in cold conditions and in the absence of oxygen-carrying proteins, by improving oxygen diffusion and energy supply to aerobic tissues. With regard to the second line of research, in the Chionodraco genus we investigated the pattern of intra- and inter- specific genetic differentiation. We found intraspecific homogeneity, but three distinct gene pools corresponding to the nominal species. We searched for putative outlier loci detecting a high level of genetic differentiation between the three species and we identified three loci, possibly influenced by natural selection, showing sequence similarity to a calmodulin transcript, an antifreeze glycoprotein/trypsinogen-like protease gene and to the mRNA of a key component of the super elongation complex. Selective pressures acting on specific loci might reflect past evolutionary processes leading to species divergence and local adaptation. The extent and timing of interspecific gene exchange was also considered to clarify the role of glacial cycles in promoting the divergence and the introgression of the Chionodraco species. We ! )! found evidences of past and present introgression: several individuals in each species showed mixed ancestry; evolutionary scenarios excluding hybridization or including it only in ancient times had small or zero posterior probabilities; data supported a scenario of interspecific gene flow associated with the two most recent interglacial periods. These findings may indicate an increased opportunity for speciation in allopatric refugia during glacial periods, followed by secondary contacts and hybridization during warmer intervals. With regard to P. antarcticum, we investigated its population genetic structure along the Antarctic Peninsula (AP), a region highly impacted by regional warming. We found a single gene pool and absence of inter-annual variability in the south-western AP, while significant differences were detected on a geographic scale from samples collected off the tip of the AP, with a signal
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