Relaxed selective constraints drove functional modifications in peripheral photoreception of the cavefish P. andruzzii and provide insight into the time of cave colonization

Calderoni, L; Rota‐Stabelli, Omar; Frigato, Elena; Panziera, Alex; Kirchner, Sandra G.; Foulkes, Nicholas S.; Kruckenhauser, Luise; Bertolucci, Cristiano; Fuselli, Silvia

doi:10.1038/hdy.2016.59

Cited by 38 publications

(31 citation statements)

References 51 publications

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“…We previously showed a general loss of light induced clock gene expression in the cavefish P. andruzzii . This lack of a gene expression response to light is due at least in part to the accumulation of loss of function mutations in key non-visual opsin photoreceptors 12 , 13 . Here we reveal the presence of additional mutations affecting a light-responsive, core circadian clock component, the per2 gene.…”

Section: Discussionmentioning

confidence: 99%

“…Troglomorphic phenotypes also include loss of body pigment, as well as reduced metabolic rate. One important cavefish model is the Somalian cavefish Phreatichthys andruzzii , which exhibits an extreme troglomorphic phenotype as the result of evolution for approximately 2,5 million years in complete isolation from sunlight beneath the desert 12 . Importantly, in a previous study, we have documented the complete loss of light entrainment of the clock in this species as well as loss-of-function mutations in three, non-visual opsin genes 12 , 13 .…”

Section: Introductionmentioning

confidence: 99%

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

Ceinos

Frigato

Pagano

et al. 2018

Sci Rep

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Light represents the principal signal driving circadian clock entrainment. However, how light influences the evolution of the clock remains poorly understood. The cavefish Phreatichthys andruzzii represents a fascinating model to explore how evolution under extreme aphotic conditions shapes the circadian clock, since in this species the clock is unresponsive to light. We have previously demonstrated that loss-of-function mutations targeting non-visual opsins contribute in part to this blind clock phenotype. Here, we have compared orthologs of two core clock genes that play a key role in photic entrainment, cry1a and per2, in both zebrafish and P. andruzzii. We encountered aberrantly spliced variants for the P. andruzzii per2 transcript. The most abundant transcript encodes a truncated protein lacking the C-terminal Cry binding domain and incorporating an intronic, transposon-derived coding sequence. We demonstrate that the transposon insertion leads to a predominantly cytoplasmic localization of the cavefish Per2 protein in contrast to the zebrafish ortholog which is distributed in both the nucleus and cytoplasm. Thus, it seems that during evolution in complete darkness, the photic entrainment pathway of the circadian clock has been subject to mutation at multiple levels, extending from opsin photoreceptors to nuclear effectors.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Ceinos

Frigato

Pagano

et al. 2018

Sci Rep

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“…See also Figure S6. suggests that P. andruzzii has been completely isolated from sunlit surface water for at least 3 million years [24,29], with the elimination of any remaining surface populations by desertification [62,63]. In this hypogean species, mutations have already affected the 6-4 and DASH photolyases, and over a sufficient evolutionary timescale, all the photolyase genes might eventually suffer loss of function or even be lost as in the case of placental mammals.…”

Section: Loss Of Photolyase Function In P Andruzziimentioning

confidence: 99%

“…For example, enhanced DNA repair has been encountered in blind cave forms of Astyanax mexicanus [25]. Our chosen cavefish model, P. andruzzii, shows a more extreme troglomorphic phenotype than A. mexicanus, even to the extent of lacking photic regulation of the circadian clock [28,29]. In order to study DNA repair function in this species, we compare it with a more genetically accessible epigean sighted species: the zebrafish, Danio rerio.…”

Section: Introductionmentioning

confidence: 99%

Modulation of DNA Repair Systems in Blind Cavefish during Evolution in Constant Darkness

et al. 2018

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Highlights d During evolution, the cavefish P. andruzzii has lost photoreactivation DNA repair d Only P. andruzzii and placental mammals are known to lack photoreactivation d The D-box enhancer coordinates DNA repair in response to ROS, UV, and visible light d Loss of D-box function in P. andruzzii underlies the lack of photoreactivation SUMMARY How the environment shapes the function and evolution of DNA repair systems is poorly understood. In a comparative study using zebrafish and the Somalian blind cavefish, Phreatichthys andruzzii, we reveal that during evolution for millions of years in continuous darkness, photoreactivation DNA repair function has been lost in P. andruzzii. We demonstrate that this loss results in part from loss-of-function mutations in pivotal DNA-repair genes. Specifically, C-terminal truncations in P. andruzzii DASH and 6-4 photolyase render these proteins predominantly cytoplasmic, with consequent loss in their functionality. In addition, we reveal a general absence of light-, UV-, and ROS-induced expression of P. andruzzii DNA-repair genes. This results from a loss of function of the D-box enhancer element, which coordinates and enhances DNA repair in response to sunlight. Our results point to P. andruzzii being the only species described, apart from placental mammals, that lacks the highly evolutionary conserved photoreactivation function. We predict that in the DNA repair systems of P. andruzzii, we may be witnessing the first stages in a process that previously occurred in the ancestors of placental mammals during the Mesozoic era.

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“…This indicates that interspecific metabolic allometry has been shaped by strong and persistent correlational selection favouring particular combinations of mass and metabolic rate within populations (Zeng 1988;Sinervo & Svensson 2002;Hunt et al 2007;White et al 2019). This pattern of multivariate stabilising selection for particular combinations of mass and metabolic rate can be considered as a type of selective constraint (Horizon 3 in Figure 1) that limits the variation in metabolic allometry (Hunt et al 2007;Calderoni et al 2016).…”

Section: An Evolutionary Genetic Approach To Metabolic Allometrymentioning

confidence: 97%

On the evolutionary physiology of metabolic allometry

Beaman¹

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All organisms rely on metabolisma complex system of biochemical reactions that either release or absorb energyto sustain life. Organisms expend energy to develop, grow, survive and reproduce. The total energy expenditure of an animal, as indicated by their metabolic rate, increases as organisms get larger. Metabolic rate, however, scales disproportionately (allometrically) with body mass, such thaton a gram for gram basissmaller organisms have a higher mass-specific metabolic rate than larger organisms. This observation has puzzled biologists for over 150 years, but progress has been made in the past few decades in explaining the origin and maintenance of metabolic allometry. The scaling relationship between mass and metabolic rate can be observed at different levels of biological organisation including over development (ontogenetic scaling), among individuals of the same developmental stage (static scaling), and among species (interspecific scaling). Importantly, there is variation in the scaling relationship between and within each of these levels and this variation has implications for the way energy flows through organisms and ecosystems, as described by metabolic theories of ecology, and for the evolution of metabolic rate and body size across the tree of life. Existing hypotheses for the variation in metabolic scaling revolve around the idea that there are universal physical constraints on the transport of metabolic inputs and outputs through circulatory networks and across tissue surfaces. The contention is that these physical constraints are I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis and have sought permission from co-authors for any jointly authored works included in the thesis.

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Relaxed selective constraints drove functional modifications in peripheral photoreception of the cavefish P. andruzzii and provide insight into the time of cave colonization

Cited by 38 publications

References 51 publications

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

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

Modulation of DNA Repair Systems in Blind Cavefish during Evolution in Constant Darkness

On the evolutionary physiology of metabolic allometry

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