Molecular evolution of cryptochromes in fishes

Mei, Qiming; Sadovy, Yvonne; Dvornyk, Volodymyr

doi:10.1016/j.gene.2015.07.086

Cited by 10 publications

(8 citation statements)

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“…Advances in genome sequencing allowed to identify circadian-related genes in several model organisms, including zebrafish. Homology-based methods allowed the identification of circadian genes in other non-model fish species [7][8][9]15]. Some studies cover the evolutionary relationships of the core-clock gene families and the mechanisms driving their molecular evolution [7][8][9][10]16], but several key questions remain open, namely on the role of paralogs, which is higher in fish when compared to other vertebrates, and its importance for adaptation of species to different environments [6].…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2021

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Background The 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. Results We identified 16 circadian-core genes in the Squalius species using a comparative transcriptomics approach. We detected evidence of positive selection in 12 of these genes using methods based on dN/dS. Positive selection was mainly found in cry and per genes of the negative loop, with 55 putatively adaptive substitutions, 16 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. We found evidence for increased nonsynonymous substitution rate in convergent lineages, likely due to positive selection at 27 sites, mostly in cry genes. Conclusions Our results support that temperature may be a 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 uncovered adaptive convergence in the southern populations, probably related to their similar thermal conditions.

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Section: Introductionmentioning

confidence: 99%

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

et al. 2021

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“…Homology-based methods allowed the identi cation of circadian genes in other non-model sh species [7][8][9]14]. Some studies cover the evolutionary relationships of the core-clock gene families and the mechanisms driving their molecular evolution [7][8][9][10]15], but several key questions remain open, namely the higher number of paralogs in sh when compared to other vertebrates, and its importance for adaptation of species to different environments [6].…”

Section: Backgroungmentioning

confidence: 99%

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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“…Another set of studies used molecular phylogenetic analyses of several major circadian clock components [ Per (Wang, ), Clk (Wang, ), Bmal (Wang, ) and Cry (Mei et al , )] in many taxa of teleost fish from different habitats, and reported significant divergence in the paralogues of these genes. Based on dN / dS ratios (Box ), it was suggested that the paralogues have diverged and are being maintained via either purifying or positive selection (Wang, , , ), whereas the evolution of Cry paralogues appears to be driven primarily by purifying selection (Mei et al , ). More studies on this topic are provided elsewhere (Young & Kay, ; Vaze & Sharma, ; Toloza‐Villalobos et al , ).…”

Section: How Do We Test Such Hypotheses?mentioning

confidence: 99%

“…Despite modern analytical tools and statistical methods (Futuyma & Bennett, ), the comparative method is strictly correlational and does not imply causality (Garland & Adolph, ; Garland et al , ). For example, experimental data show that Cry paralogues have evolved across teleost fish originating from different habitats (Mei et al , ). Although these data are taken to suggest that some factors in the ecology of fish drove this divergence, this is only a correlation‐based hypothesis and one cannot establish causality between different habitats and the divergence of Cry .…”

Section: How Do We Test Such Hypotheses?mentioning

confidence: 99%

On the relevance of using laboratory selection to study the adaptive value of circadian clocks

Abhilash

Sharma

2016

Physiol. Entomol.

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Abstract. The phrase 'as sure as night comes after day' highlights the most conspicuous phenomenon on earth (i.e. the daily cycling of geophysical factors). It is hypothesized that life-forms on earth have evolved timekeeping mechanisms (circadian clocks) as adaptations to cope with such cyclic variations in their environment and, to test this hypothesis, diverse strategies have been employed. In this review, these different approaches, including comparative, clinal, ecology and/or trait manipulation and laboratory selection strategies are discussed, aiming to evaluate the adaptive value of circadian clocks. The limitations of each of these methods are assessed, and it is suggested that laboratory selection is an ideal, potent and suitable strategy for examining whether circadian clocks are indeed adaptations. In support of this, laboratory selection strategies are highlighted and critically reviewed in a discussion of studies that demonstrate the evolution of circadian clocks and life-history traits in response to selection for the timing of rhythmic behaviours, as well as those studies that demonstrate the evolution of circadian clocks in response to selection for life-history traits. Finally, newer approaches are proposed that involve the use of mutants, simultaneous manipulation of multiple environmental factors and genomic technologies in conjunction with laboratory selection to further explore the adaptive significance of circadian clocks.

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Molecular evolution of cryptochromes in fishes

Cited by 10 publications

References 64 publications

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

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

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

On the relevance of using laboratory selection to study the adaptive value of circadian clocks

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