Regressive evolution in Somalian Cavefish Phreatichthys andruzzii : loss of selective constraint on opsin genes

Phreatichthys andruzzii is a Somalian cavefish that evolved in complete isolation and absence of light beneath the desert for about two million years. Constant darkness caused extreme degenerative phenotypes, such as complete depigmentation, reduced metabolic rate and complete eye degeneration. The circadian clock is partially degenerated in this cavefish, and mutations in several photoreceptors and clock-related genes play roles in its lack of response to light. However, a detailed description of the molecular mechanisms underlying the regression of this important mechanism is still missing. We investigated the molecular evolution of the non-visual photoreceptor melanopsin Opn4m2, whose premature stop codon accounts for the inability of the peripheral clock to respond to light. To test the hypothesis that other light-related mechanisms are undergoing degeneration, we studied the molecular evolution of the visual pigment rhodopsin, expressed in the brain of P. andruzzii and probably involved in its photophobic behavior. The same genes were studied in another blind cavefish, Garra barreimiae from Oman, a close relative to P. andruzzii that independently colonized subterranean waters and evolved troglomorphic traits. Our results based on within and between species analyses, and on time estimation of pseudogenization, show that both genes lost signature of selective constraints in P. andruzzii. Conversely, in G. barreimiae, that colonized the cave environment more recently and lacks complete isolation from the surface, the genes are still conserved. Our observations indicate that the long and extreme isolation of P. andruzzii in darkness led to a general relaxation of natural selection on light-responsive physiological mechanisms.