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Agostini, Cecilia (2014) Transcriptomics and population differentiation in two notothenioid Antarctic fish. [Tesi di dottorato]

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Abstract (inglese)

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 remodeling 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 of increased fragmentation over time. The reduced level of gene flow along the shelf, the increase of differentiation through time, and the inability to capture P. antarcticum in the central-western AP for two consecutive years, all suggest that this sea ice dependent species has been affected by climate change with possible cascading effects on the Antarctic marine food web.

Abstract (italiano)

I nototenioidei antartici si sono evoluti per milioni di anni nelle acque gelide che caratterizzano l’Oceano Meridionale; essi presentano una vasta gamma di adattamenti per resistere al freddo e ora dominano la fauna ittica antartica sia per numero di specie che per biomassa. Per la loro estrema stenotermia, questi pesci potrebbero essere fortemente vulnerabili ai cambiamenti climatici con possibili effetti a cascata sull’intero ecosistema marino antartico. Pertanto, è di fondamentale importanza investigare le basi genetiche e genomiche dell’adattamento al freddo, analizzare i processi di differenziamento derivanti dai cambiamenti climatici del passato e attuali e, allo stesso tempo, indagare il livello di variabilità e di differenziamento genetico presente a livello di specie e di popolazione. In questo dottorato sono state prese in considerazione quattro specie di nototenioidei antartici: le tre specie di derivazione recente appartenenti al genere Chionodraco, Chionodraco hamatus, Chionodraco rastrospinosus e Chionodraco myersi, e Pleuragramma antarcticum. Il genere Chionodraco appartiene alla famiglia Channichthyidae (icefish), unica tra i vertebrati per l’assenza di emoglobina e l’incapacità di esprimere mioglobina nel muscolo scheletrico. Un adeguato rifornimento di ossigeno ai tessuti è permesso da un marcato rimodellamento del sistema cardio-vascolare e da un’elevata densità mitocondriale a livello muscolare. P. antarcticum (Nototheniidae) è l'unico nototenioideo caratterizzato da un ciclo vitale completamente pelagico, è dipendente dal ghiaccio marino e svolge un ruolo chiave nella catena trofica dell’ecosistema marino antartico. Le analisi svolte in questo dottorato possono essere raggruppate in due principali linee di ricerca: 1) l'approfondimento della conoscenza sulle basi genetiche e genomiche dell’adattamento al freddo degli icefish; 2) l'analisi del pattern di differenziamento genetico presente a livello intra- e inter-specifico, con particolare enfasi su come le condizioni ambientali del passato e del presente abbiano plasmato e stiano influenzando la struttura genetica delle specie. Per quanto riguarda la prima linea di ricerca, è stato ricostruito e annotato il primo trascrittoma normalizzato del muscolo scheletrico di C. hamatus e l’informazione di sequenza così ottenuta è stata utilizzata per verificare l'ipotesi di duplicazione di geni coinvolti nella funzione mitocondriale. Utilizzando una pipeline bioinformatica sviluppata ad hoc, sono stati identificati 124 geni duplicati specifici del lineage di C. hamatus. La proporzione di duplicazioni lineage-specifiche identificate in C. hamatus è risultata significativamente maggiore a quella presente in specie modello di pesci teleostei. Un’analisi di arricchimento funzionale ha mostrato come l’insieme dei geni duplicati in C. hamatus fosse significativamente arricchito in proteine con localizzazione mitocondriale, coinvolte nella funzione e nella biogenesi mitocondriale. La presenza di elevate densità mitocondriali e il mantenimento a livello genomico di geni duplicati con funzione mitocondriale potrebbero conferire un vantaggio selettivo agli icefish in un ambiente freddo e in assenza di proteine di trasporto per l’ossigeno, migliorando la diffusione dell’ossigeno e la produzione di energia nei tessuti aerobici. Per quanto riguarda la seconda linea di ricerca, è stato studiato il pattern di differenziamento genetico presente a livello intra- e inter-specifico nel genere Chionodraco. E’ stata rilevata omogeneità intraspecifica, ma la presenza di tre pool genici distinti corrispondenti alle tre specie. Sono stati ricercati putativi loci outlier, in grado di rilevare un elevato livello di differenziamento genetico tra specie. Sono stati identificati tre loci, probabilmente soggetti a selezione naturale, con similarità di sequenza per la calmodulina, per una proteasi antifreeze glycoprotein/trypsinogen-like e per un componente fondamentale del super elongation complex. Pressioni selettive, agenti su loci specifici, potrebbero riflettere processi evolutivi del passato che hanno portato alla divergenza tra specie e all’adattamento locale. È stata inoltre investigata la presenza e l’entità del flusso genico, passato e presente, tra le tre specie del genere Chionodraco, anche per chiarire il ruolo dei cicli glaciali nel processo di divergenza e d’introgressione tra specie. Sono state rilevate molteplici evidenze d’introgressione, associata ai due periodi interglaciali più recenti (Eemiano e Olocene), che potrebbe indicare una maggiore opportunità di speciazione allopatrica in rifugi durante i periodi glaciali, seguita da contatti secondari e ibridazione durante gli intervalli più caldi. Nella specie P. antarcticum, è stata studiata la struttura genetica di popolazione a livello della Penisola Antartica, una regione molto influenzata dal surriscaldamento climatico. Lungo la costa sud-occidentale della penisola è stato rilevato un pool genico unico e assenza di variabilità su scala temporale. Differenze significative sono state evidenziate, invece, su scala geografica tra campioni raccolti nella regione sud-occidentale e quelli ottenuti dalla punta settentrionale della penisola, con un segnale di incremento del differenziamento nel tempo. Molteplici evidenze, quali il ridotto livello di flusso genico lungo la piattaforma continentale della penisola, l'aumento del differenziamento su scala temporale e l'incapacità di catturare P. antarcticum lungo la costa centro-occidentale per due anni consecutivi, suggeriscono che questa specie, dipendente dal ghiaccio marino, sia stata colpita dai cambiamenti climatici con possibili effetti a cascata sull’intera catena alimentare dell’ecosistema marino antartico.

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Tipo di EPrint:Tesi di dottorato
Relatore:Zane, Lorenzo
Dottorato (corsi e scuole):Ciclo 26 > Scuole 26 > BIOSCIENZE E BIOTECNOLOGIE > BIOLOGIA EVOLUZIONISTICA
Data di deposito della tesi:25 Gennaio 2014
Anno di Pubblicazione:25 Gennaio 2014
Parole chiave (italiano / inglese):Notothenioidei, icefish, Chionodraco, Antarctic silverfish, genetica di popolazione/ population genetics, evoluzione del genoma/genome evolution, adattamento al freddo/cold adaptation, duplicazione genica/gene duplication, cambiamenti climatici/ climate change, marcatori microsatellite/microsatellite markers, ibridazione/hybridization, selezione naturale/natural selection
Settori scientifico-disciplinari MIUR:Area 05 - Scienze biologiche > BIO/07 Ecologia
Struttura di riferimento:Dipartimenti > Dipartimento di Biologia
Codice ID:6365
Depositato il:03 Nov 2014 09:54
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