title: Relaxed selective constraints drove functional modifications in peripheral photoreception of the cavefish P. andruzzii and provide insight into the time of cave colonization.
abstract: 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.
authors.affiliation: Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy.
authors.forename: L
authors.initials: L
authors.lastname: Calderoni
authors.affiliation: Research and Innovation Centre, Fondazione Edmund Mach, San Michele all'Adige, Italy.
authors.forename: O
authors.initials: O
authors.lastname: Rota-Stabelli
authors.affiliation: Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy.
authors.forename: E
authors.initials: E
authors.lastname: Frigato
authors.affiliation: Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy.|Department of Biodiversity and Molecular Ecology, Fondazione Edmund Mach, San Michele all'Adige, Italy.
authors.forename: A
authors.initials: A
authors.lastname: Panziera
authors.affiliation: Central Research Laboratories, Museum of Natural History of Vienna, Vienna, Austria.
authors.forename: S
authors.initials: S
authors.lastname: Kirchner
authors.affiliation: Institute of Toxicology and Genetics, Karlsruhe Institute of Technology, Karlsruhe, Germany.
authors.forename: N S
authors.initials: NS
authors.lastname: Foulkes
authors.affiliation: Central Research Laboratories, Museum of Natural History of Vienna, Vienna, Austria.
authors.forename: L
authors.initials: L
authors.lastname: Kruckenhauser
authors.affiliation: Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy.
authors.forename: C
authors.initials: C
authors.lastname: Bertolucci
authors.affiliation: Department of Life Sciences and Biotechnology, University of Ferrara, Ferrara, Italy.
authors.forename: S
authors.initials: S
authors.lastname: Fuselli
mesh_terms: D000818:Animals; D005075:Biological Evolution; D059552:Caves; D057906:Circadian Clocks; D003530:Cyprinidae / Q000235:genetics* / Q000502:physiology; D019143:Evolution, Molecular; D029941:Fish Proteins / Q000235:genetics; D008027:Light; D010641:Phenotype; D012243:Rhodopsin / Q000235:genetics; D017299:Rod Opsins / Q000235:genetics*; D012641:Selection, Genetic; D000099210:Melanopsin
chemical_list: D029941:Fish Proteins; D012243:Rhodopsin; D017299:Rod Opsins; D000099210:Melanopsin