Parallel Evolution of Opsin Gene Expression in African Cichlid Fishes

Abstract

Phenotypic evolution may occur either through alterations to the structure of protein-coding genes or their expression. Evidence for which of these two mechanisms more commonly contribute to the evolution of a phenotype can be garnered from examples of parallel and convergent evolution. The visual system of East African cichlid fishes is an excellent system with which to address this question. Cichlid fishes from Lakes Malawi (LM) and Victoria together exhibit three diverse palettes of coexpressed opsins and several important protein-coding mutations that both shift spectral sensitivity. Here we assess both opsin expression and protein-coding diversity among cichlids from a third rift lake, Lake Tanganyika (LT). We found that Tanganyikan cichlids exhibit three palettes of coexpressed opsins that largely overlap the short-, middle-, and long-wavelength-sensitive palettes of LM cichlids. Bayesian phenotypic clustering and ancestral state reconstructions both support the parallel evolution of the short- and middle-wavelength palettes among cichlids from LT and LM. In each case, these transitions occurred from different ancestors that expressed the same long-wavelength palette. We also identified similar but distinct patterns of correlated evolution between opsin expression, diet, and lens transmittance among cichlids from LT and LM as well. In contrast to regulatory changes, we identified few functional or potentially functional mutations in the protein-coding sequences of three variable opsins, with the possible exception of the SWS1 (ultraviolet) opsin. These results underscore the important contribution that gene regulation can make to rapid phenotypic evolution and adaptation.

Optical advantages and function of multifocal spherical fish lenses

“…The evolutionary adaptation of visual pigments occurs by genetic changes, either in the expression of pigment genes [46] or mutations in the opsin genes leading to amino acid substitutions in the opsin molecule [47][48][49][50][51]. Here we have shown that the optical properties of the lens should match the spectral composition of the retina in order to maximize optical performance, indicating that there should be an equally large variation in the optical properties of fish lenses, and this has indeed been observed [10,11,[37][38][39][40].…”

Evolution of bower building in Lake Malawi cichlid fish: phylogeny, morphology, and behavior

“…In particular, the Lake Malawi flock has over 500 species that evolved within the last 5 million years, displaying one of the most rapid rates of speciation known amongst vertebrates (Brawand et al, 2014). Cichlids are renowned for their high levels of phenotypic diversity across many well-studied traits including jaw and trophic morphology (Kassam et al, 2004;Albertson et al, 2005;Hulsey et al, 2006;Muschick et al, 2011;Gunter et al, 2013), vision O'Quin et al, 2010), and sex determination (Roberts et al, 2009;Parnell and Streelman, 2013). Although it is wellknown that these species also exhibit many remarkably diverse patterns of behavior, systematic analyses of these traits across taxa are rare (Barlow, 2008).…”

Modulation of environmental light alters reception and production of visual signals in Nile tilapia

“…Nile tilapia form an ancestral outgroup to the lacustrine African cichlids (Kocher, 2004), and are a growing presence in laboratory research (El-Sayed, 2006). Cichlid fish show variation in signal reception, as visual pigment complements show a great range of natural variation (Carleton and Kocher, 2001;Parry et al, 2005;Sabbah et al, 2010;O'Quin et al, 2010). Additionally, cichlids are notorious for their variation in signal production, showing myriad behaviours (Barlow, 2000) and body colourations (Kornfield and Smith, 2000), many of which are species specific (Hofmann et al, 2009).…”