Mutations in blind cavefish target the light-regulated circadian clock gene, period 2

Ceinos, Rosa M.; Frigato, Elena; Pagano, Cristina; Fröhlich, Nadine; Negrini, Pietro; Cavallari, Nicola; Vallone, Daniela; Fuselli, Silvia; Bertolucci, Cristiano; Foulkes, Nicholas S.

doi:10.1038/s41598-018-27080-2

Cited by 28 publications

(22 citation statements)

References 40 publications

(63 reference statements)

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“…Moreover, these changes can impact protein structure as certain amino acids present a propensity for speci c structural arrangements [44]. The fact that we nd positive selection in the negative elements is in line with previous studies showing that mutations in PER2 protein were important for the adaptation of blind cave sh to its environment [45]. Taken together, these results suggest that circadian system genes were involved in Iberian Squalius species adaptation, which occurred mostly by changes in the negative elements of the circadian system.…”

Section: Evidence Of Positive Selection Is Related With Protein Predisupporting

confidence: 91%

Adaptation and convergence in circadian-related genes in Iberian freshwater fish

Moreno

Jesus

Sousa³

et al. 2020

Preprint

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BackgroundThe circadian clock is a biological timing system that improves the ability of organisms to deal with environmental fluctuations. At the molecular level it consists of a network of transcription-translation feedback loops, involving genes that activate (bmal and clock – positive loop) and repress expression (cryptochrome (cry) and period (per) – negative loop). This is regulated by daily alternations of light but can also be affected by temperature. Fish, as ectothermic, depend on the environmental temperature and thus are good models to study its integration within the circadian system. Here, we studied the molecular evolution of circadian genes in four Squalius freshwater fish species, distributed across Western Iberian rivers affected by two climatic types with different environmental conditions (e.g. light and temperature). S. carolitertii and S. pyrenaicus inhabit the colder northern region under Atlantic climate type, while S. torgalensis, S. aradensis and some populations of S. pyrenaicus inhabit the warmer southern region affected by summer droughts, under Mediterranean climate type. ResultsWe identified 16 circadian-core genes in the Squalius species using a comparative transcriptomics approach. We detected evidence of positive selection in nine of these genes using methods based on dN/dS. Positive selection was mainly found in cry and per genes of the negative loop of the cycle, with 11 putatively adaptive substitutions mostly located on protein domains. Evidence for positive selection is predominant in southern populations affected by the Mediterranean climate type. By predicting protein features we found that changes at sites under positive selection can impact protein thermostability by changing their aliphatic index and isoelectric point. Additionally, in nine genes, the phylogenetic clustering of species that belong to different clades but inhabit southern basins with similar environmental conditions indicated evolutionary convergence.ConclusionsOur results support that temperature may be a strong selective pressure driving the evolution of genes involved in the circadian system. By integrating sequence-based functional protein prediction with dN/dS-based methods to detect selection we also uncovered adaptive convergence in the southern populations, probably related to their similar thermal conditions.

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Section: Evidence Of Positive Selection Is Related With Protein Predisupporting

confidence: 91%

Adaptation and convergence in circadian-related genes in Iberian freshwater fish

Moreno

Jesus

Sousa³

et al. 2020

Preprint

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“…Such rhythms usually disappear in constant conditions, light or darkness (Feliciano et al, 2011; Nisembaum et al, 2012; Vera et al, 2013), showing that per2a rhythmicity is strongly dependent of the LD cycle. Indeed, it is well-known that per2a is a light-induced gene with a key role in the molecular mechanism that entrains the LEOs in zebrafish (Vatine et al, 2011; Moore and Whitmore, 2014; Ben-Moshe et al, 2014; Ceinos et al, 2018). Our results support this role of per2a as a light-dependent clock gene also in goldfish.…”

Section: Discussionmentioning

confidence: 99%

Time-Lag in Feeding Schedule Acts as a Stressor That Alters Circadian Oscillators in Goldfish

et al. 2018

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The circadian system controls temporal homeostasis in all vertebrates. The light-dark (LD) cycle is the most important zeitgeber (“time giver”) of circadian system, but feeding time also acts as a potent synchronizer in the functional organization of the teleost circadian system. In mammals is well known that food intake during the rest phase promotes circadian desynchrony which has been associated with metabolic diseases. However, the impact of a misalignment of LD and feeding cycles in the entrainment of fish circadian oscillators is largely unknown. The objective of this work was to investigate how a time-lag feeding alters temporal homeostasis and if this could be considered a stressor. To this aim, goldfish maintained under a 12 h light-12 h darkness were fed at mid-photophase (SF6) or mid-scotophase (SF18). Daily rhythms of locomotor activity, clock genes expression in hypothalamus, liver, and head kidney, and circulating cortisol were studied. Results showed that SF6 fish showed daily rhythms of bmal1a and clock1a in all studied tissues, being in antiphase with rhythms of per1 genes, as expected for proper functioning clocks. The 12 h shift in scheduled feeding induced a short phase advance (4–5-h) of the clock genes daily rhythms in the hypothalamus, while in the liver the shift for clock genes expression rhythms was the same that the feeding time shift (∼12 h). In head kidney, acrophases of per genes underwent a 12-h shift in SF18 animals, but only 6 h shift for clock1a. Plasma cortisol levels showed a significant daily rhythm in animals fed at SF6, but not in SF18 fish fed, which displayed higher cortisol values throughout the 24-h. Altogether, results indicate that hypothalamus, liver, and head kidney oscillate in phase in SF6 fish, but these clocks are desynchronized in SF18 fish, which could explain cortisol alterations. These data reinforce the hypothesis that the misalignment of external cues (daily photocycle and feeding time) alters fish temporal homeostasis and it might be considered a stressor for the animals.

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“…Cavefish have developed a series of unique physical and behavioral features in their adaptation to cave habitats, including reduction of eyesight and pigmentation, sensitive sensory organs, unique dietary preferences, and predation behavior (Jeffery, 2009). In recent years, many research related to morphology, molecular biology and ecology has been conducted on various cavefish species such as Astyanax mexicanus (Varatharasan et al, 2009;Hyacinthe et al, 2019) and Phreatichthys andruzzii (Ceinos et al, 2018). However, due to difficulties in adequately sampling wild cavefish species, clear understanding of regulatory mechanisms underlying their adaptive traits requires further investigation (Zagmajster et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Comparative Transcriptomics Reveals the Molecular Genetic Basis of Cave Adaptability in Sinocyclocheilus Fish Species

Zhao

Chen

et al. 2020

Front. Ecol. Evol.

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Cavefish evolved a series of distinct survival mechanisms for adaptation to cave habitat. Such mechanisms include loss of eyesight and pigmentation, sensitive sensory organs, unique dietary preferences, and predation behavior. Thus, it is of great interest to understand the mechanisms underlying these adaptability traits of troglobites. The teleost genus Sinocyclocheilus (Cypriniformes: Cyprinidae) is endemic to China and has more than 70 species reported (including over 30 cavefish species). High species diversity and diverse phenotypes make the Sinocyclocheilus as an outstanding model for studying speciation and adaptive evolution. In this study, we conducted a comparative transcriptomics study on the brain tissues of two Sinocyclocheilus species (surface-dwelling species-Sinocyclocheilus malacopterus and semi-cavedwelling species-Sinocyclocheilus rhinocerous living in the same water body. A total of 425,188,768 clean reads were generated, which contributed to 102,839 Unigenes. Bioinformatic analysis revealed a total of 3,289 differentially expressed genes (DEGs) between two species Comparing to S. malacopterus, 2,598 and 691 DEGs were found to be respectively, down-regulated and up-regulated in S. rhinocerous. Furthermore, it is also found tens of DEGs related to cave adaptability such as insulin secretion regulation (MafA, MafB, MafK, BRSK, and CDK16) and troglomorphic traits formation (CEP290, nmnat1, coasy, and pqbp1) in the cave-dwelling S. rhinocerous. Interestingly, most of the DEGs were found to be down-regulated in cavefish species and this trend of DEGs expression was confirmed through qPCR experiments. This study would provide an appropriate genetic basis for future studies on the formation of troglomorphic traits and adaptability characters of troglobites, and improve our understanding of mechanisms of cave adaptation.

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Mutations in blind cavefish target the light-regulated circadian clock gene, period 2

Cited by 28 publications

References 40 publications

Adaptation and convergence in circadian-related genes in Iberian freshwater fish

Adaptation and convergence in circadian-related genes in Iberian freshwater fish

Time-Lag in Feeding Schedule Acts as a Stressor That Alters Circadian Oscillators in Goldfish

Comparative Transcriptomics Reveals the Molecular Genetic Basis of Cave Adaptability in Sinocyclocheilus Fish Species

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