Eye degeneration in the blind cave-dwelling fish <i>Phreatichthys andruzzii</i>

Berti, Roberto; Durand, J.; Becchi, Samuele; Brizzi, R.; Keller, Nicole; Ruffat, Gisèle

doi:10.1139/z01-084

Cited by 30 publications

(41 citation statements)

References 8 publications

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“…The adult fishes completely lack eyes, pigments and scales and their metabolic rate is extremely reduced. In particular, the eye is totally regressed 36 h post fertilization and 1 month later there remains only a rudimentary cyst, with loss of the optic nerves and strongly reduced optic lobes (Berti et al, 2001;Stemmer et al, 2015). This degeneration is rather premature compared, for example, with what is known for the blind Mexican cavefish Astyanax mexicanus.…”

Section: Introductionmentioning

confidence: 94%

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

et al. 2016

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The genetic basis of phenotypic changes in extreme environments is a key but rather unexplored topic in animal evolution. Here we provide an exemplar case of evolution by relaxed selection in the Somalian cavefish Phreatichthys andruzzii that has evolved in the complete absence of light for at least 2.8 million years. This has resulted in extreme degenerative phenotypes, including complete eye loss and partial degeneration of the circadian clock. We have investigated the molecular evolution of the nonvisual photoreceptor melanopsin opn4m2, whose mutation contributes to the inability of peripheral clocks to respond to light. Our intra-and inter-species analyses suggest that the 'blind' clock in P. andruzzii evolved because of the loss of selective constraints on a trait that was no longer adaptive. Based on this change in selective regime, we estimate that the functional constraint on cavefish opn4m2 was relaxed at ∼ 5.3 Myr. This implies a long subterranean history, about half in complete isolation from the surface. The visual photoreceptor rhodopsin, expressed in the brain and implicated in photophobic behavior, shows similar evolutionary patterns, suggesting that extreme isolation in darkness led to a general weakening of evolutionary constraints on light-responsive mechanisms. Conversely, the same genes are still conserved in Garra barreimiae, a cavefish from Oman, that independently and more recently colonized subterranean waters and evolved troglomorphic traits. Our results contribute substantially to the open debate on the genetic bases of regressive evolution.

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Section: Introductionmentioning

confidence: 94%

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

et al. 2016

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“…Phreatichthys andruzzii is a member of the Cyprinidae family and inhabits subterranean cave systems in desert areas of central Somalia. It is a typical cave-dwelling vertebrate, showing an extreme troglomorphic phenotype with complete anophthalmy, together with the complete absence of optic nerves and chiasma, and an extreme reduction in size of the mesencephalic lobes (Ercolini and Berti, 1975;Berti et al, 2001). We have recently demonstrated that mutations in two widely expressed non-visual opsins, a melanopsin and a teleost multiple tissue (TMT)-opsin orthologue, are responsible for the blind clock phenotype in P. andruzzii (Cavallari et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Encephalic photoreception and phototactic response in the troglobiont Somalian blind cavefish Phreatichthys andruzzii

Tarttelin

Frigato

Bellingham

et al. 2012

Journal of Experimental Biology

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SUMMARYMany physiological and behavioural responses to changes in environmental lighting conditions are mediated by extraocular photoreceptors. Here we investigate encephalic photoreception in Phreatichthys andruzzii, a typical cave-dwelling fish showing an extreme phenotype with complete anophthalmy and a reduction in size of associated brain structures. We firstly identified two P. andruzzii photopigments, orthologues of rod opsin and exo-rod opsin. In vitro, both opsins serve as light-absorbing photopigments with  max around 500nm when reconstituted with an A 1 chromophore. When corrected for the summed absorption from the skin and skull, the spectral sensitivity profiles shifted to longer wavelengths (rod opsin: 521nm; exo-rod opsin: 520nm). We next explored the involvement of both opsins in the negative phototaxis reported for this species. A comparison of the spectral sensitivity of the photophobic response with the putative A 2 absorbance spectra corrected for skin/skull absorbance indicates that the A 2 versions of either or both of these pigments could explain the observed behavioural spectral sensitivity.

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“…An unresolved issue in this study is the identification of the sensory modality involved in numerical discrimination. Because P. andruzzii shows a complete anophthalmy (Berti et al, 2001), only the use of another sensory modality can be advocated to explain the results we obtained. The two main candidates are the sense of touch and the lateral line system.…”

Section: Discussionmentioning

confidence: 89%

“…Selective pressures might have acted differently from other fish species, on the one hand reducing the cerebral mass in order to optimize the metabolic consumption of the brain, and on the other hand losing the neural circuits supporting cognitive functions not useful in the cave, such as those necessary to discriminate the larger shoal (Buckingham et al, 2007;Gómez-Laplaza and Gerlai, 2011b;Hager and Helfman, 1991). Phreatichthys andruzzii shows an extreme troglomorphic phenotype, and the complete anophthalmy is accompanied by the complete absence of optic nerves and chiasm and by a strong reduction in the size of the entire brain (Berti et al, 2001;Ercolini and Berti, 1975). Furthermore, the schooling behavior is significantly reduced in the cave forms of Astyanax mexicanus relative to the surface form (Kowalko et al, 2013;Parzefall, 1983).…”

Section: Research Articlementioning

confidence: 99%

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Non-visual numerical discrimination in a blind cavefish (Phreatichthys andruzzii)

Bisazza

Tagliapietra

Bertolucci

et al. 2014

Journal of Experimental Biology

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Over a decade of comparative studies, researchers have found that rudimentary numerical abilities are widespread among vertebrates. While experiments in mammals and birds have employed a variety of stimuli (visual, auditory and tactile), all fish studies involved visual stimuli and it is unknown whether fish can process numbers in other sensory modalities. To fill this gap, we studied numerical abilities in Phreatichthys andruzzii, a blind cave-dwelling species that evolved in the phreatic layer of the Somalia desert. Fish were trained to receive a food reward to discriminate between two groups of objects placed in opposite positions of their home tank. In Experiment 1, subjects learned to discriminate between two and six objects, with stimuli not controlled for non-numerical continuous variables that covary with numbers, such as total area occupied by stimuli or density. In Experiment 2, the discrimination was two versus four, with half of the stimuli controlled for continuous quantities and half not controlled for continuous quantities. The subjects discriminated only the latter condition, indicating that they spontaneously used non-numerical information, as other vertebrates tested in similar experiments. In Experiments 3 and 4, cavefish trained from the beginning only with stimuli controlled for continuous quantities proved able to learn the discrimination of quantities based on the sole numerical information. However, their numerical acuity was lower than that reported in other teleost fish tested with visual stimuli.

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Eye degeneration in the blind cave-dwelling fish Phreatichthys andruzzii

Cited by 30 publications

References 8 publications

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

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

Encephalic photoreception and phototactic response in the troglobiont Somalian blind cavefish Phreatichthys andruzzii

Non-visual numerical discrimination in a blind cavefish (Phreatichthys andruzzii)

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