The Eyes Have It: Regulatory and Structural Changes Both Underlie Cichlid Visual Pigment Diversity

Hofmann, Christopher M.; O’Quin, Kelly E.; Marshall, N. Justin; Cronin, Thomas W.; Seehausen, Ole; Carleton, Karen L.

doi:10.1371/journal.pbio.1000266

Cited by 158 publications

(327 citation statements)

References 66 publications

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“…S1). Five of these sites also differed in physical properties between one another, making them prime candidates for sites under adaptive divergence by spectral tuning (29) (Fig. S1).…”

Section: Resultsmentioning

confidence: 99%

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Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes

Cortesi

Musilová

Stieb

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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145

212

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Single-gene and whole-genome duplications are important evolutionary mechanisms that contribute to biological diversification by launching new genetic raw material. For example, the evolution of animal vision is tightly linked to the expansion of the opsin gene family encoding light-absorbing visual pigments. In teleost fishes, the most species-rich vertebrate group, opsins are particularly diverse and key to the successful colonization of habitats ranging from the bioluminescence-biased but basically dark deep sea to clear mountain streams. In this study, we report a previously unnoticed duplication of the violet-blue short wavelength-sensitive 2 (SWS2) opsin, which coincides with the radiation of highly diverse percomorph fishes, permitting us to reinterpret the evolution of this gene family. The inspection of close to 100 fish genomes revealed that, triggered by frequent gene conversion between duplicates, the evolutionary history of SWS2 is rather complex and difficult to predict. Coincidentally, we also report potential cases of gene resurrection in vertebrate opsins, whereby pseudogenized genes were found to convert with their functional paralogs. We then identify multiple novel amino acid substitutions that are likely to have contributed to the adaptive differentiation between SWS2 copies. Finally, using the dusky dottyback Pseudochromis fuscus, we show that the newly discovered SWS2A duplicates can contribute to visual adaptation in two ways: by gaining sensitivities to different wavelengths of light and by being differentially expressed between ontogenetic stages. Thus, our study highlights the importance of comparative approaches in gaining a comprehensive view of the dynamics underlying gene family evolution and ultimately, animal diversification.

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“…S1). Five of these sites also differed in physical properties between one another, making them prime candidates for sites under adaptive divergence by spectral tuning (29) (Fig. S1).…”

Section: Resultsmentioning

confidence: 99%

“…S1). A functional analysis of the percomorph-specific SWS2A duplicates was conducted in the dusky dottyback using a combination of MSP (36) and qRT-PCR approaches (29) (Fig. 3 D and E and Table S2).…”

Section: Methodsmentioning

confidence: 99%

Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes

Cortesi

Musilová

Stieb

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

145

212

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“…For example fish living in turbid waters, which are rich in longer wavelength, have generally lost their short-sensitive opsin genes, do not express them or have visual pigments shifted to match their light environments (Yokoyama et al, 1999;Terai et al, 2002;Sugawara et al, 2005;Seehausen et al, 2008;Hofmann et al, 2009). More recent research indicates selection from the light environment could also be driving the evolution of opsin expression in birds (Bloch, 2015).…”

Section: Why Study Opsins?mentioning

confidence: 99%

The evolution of opsins and color vision: connecting genotype to a complex phenotype

Bloch¹

2016

Acta biol. Colomb.

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Este artículo fue presentado por invitación de la Red Colombiana de Biología Evolutiva (COLEVOL) y Acta Biológica Colombiana con el fin de incentivar la investigación en el área de biología evolutiva. ABSTRACTDissecting the genetic basis of adaptive traits is key to our understanding of evolutionary processes. A major and essential step in the study of evolutionary genetics is drawing link between genotype and phenotype, which depends on the difficult process of defining the phenotype at different levels, from functional to organismal. Visual pigments are a key component of the visual system and their evolution could also provide important clues on the evolution of visual sensory system in response to sexual and natural selection. As a system in which genotype can be linked to phenotype, I will use visual pigments and color vision, particularly in birds, as a case of a complex phenotype. I aim to emphasize the difficulties in drawing the genotype-phenotype relationship for complex phenotypes and to highlight the challenges of doing so for color vision. The use of vision-based receiver models to quantify animal colors and patterns is increasingly important in many fields of evolutionary research, spanning studies of mate choice, predation, camouflage and sensory ecology. Given these models impact on evolution and ecology, it is important to provide other researchers with the opportunity to better understand animal vision and the corresponding advantages and limitations of these models.Keywords: avian visual pigments, color vision, complex phenotypes, genotype-phenotype, opsins. RESUMENEntender la base genética de los rasgos adaptativos es un paso crítico en el estudio de los procesos evolutivos. Para estudiar la conexión entre genotipo y fenotipo es importante definir el fenotipo a diferentes niveles: desde las proteínas que se construyen con base en un gen, hasta las características finales presentes en un organismo. Las opsinas y los fotopigmentos son elementos primordiales de la visión y entender cómo han evolucionado es fundamental en el estudio de la visión en los animales como un caracter derivado de selección natural o sexual. Este artículo se enfoca en este sistema, en el que se pueden conectar genotipo y fenotipo, como ejemplo de fenotipo complejo para ilustrar las dificultades de establecer una relación clara entre genotipo y fenotipo. Adicionalmente, este artículo tiene como objetivo discutir el funcionamiento del sistema de fotorrecepción, con énfasis particular en las aves, con el fin de enumerar varios factores que deben ser tenidos en cuenta para predecir cambios en la visión a partir del estudio de los fotopigmentos. Dado que los modelos basados en la visión de aves son cada vez más usados en diversas áreas de la biología evolutiva tales como: selección de pareja, depredación y camuflaje; se hace relevante entender los fundamentos y limitaciones de estos modelos. Por esta razón, en este artículo discuto los detalles y aspectos prácticos del uso de los modelos de visión existentes para aves, con el...

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“…In fishes, spatial segregation is a more common mechanism of coexistence, and concomitant spatial segregation in activity rhythms and different eye sizes has been observed in several ecologically equivalent and sympatric species. In cichlids of African lakes, vision greatly contributes to their habitat segregation and even to their speciation (Seehausen et al 2008, Hofmann et al 2009). In this family, 2 highly morphologically similar species, Haplochromis hiatus and H. iris, prey on similar food items and inhabit different depths.…”

Section: Sensory Specialisationmentioning

confidence: 99%

Sensory constraints in temporal segregation in two species of anglerfish, Lophius budegassa and L. piscatorius

Colmenero¹,

Aguzzi²,

Lombarte³

et al. 2010

Mar. Ecol. Prog. Ser.

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The temporal segregation of 2 ecologically equivalent and sympatric species, the black anglerfish Lophius budegassa and white anglerfish L. piscatorius, was studied in relation to day-night behaviour and the underlying morphological variation in the sensory organs. Temporally scheduled trawl sampling was conducted on the western Mediterranean shelf, and diel fluctuations in catches were used as a proxy of behavioural rhythms. L. budegassa was more abundant at night than L. piscatorius, which mostly occurred in daytime catches. The observed differences in the timing of maximum activity (i.e. catches) were consistent with differences in otolith sagittae weight, eye/lens sizes and optical sensitivity. L. budegassa presented significantly heavier otolith sagittae than L. piscatorius, indicating that the behaviour of the black anglerfish is mostly acoustically driven (a typical characteristic of species living in dim light conditions). Preference for a dim light environment was also confirmed by the high optical sensitivity observed in this species achieved by enlarging the photoreceptors' diameter. In contrast, L. piscatorius showed larger eyes and lenses than L. budegassa, but only in individuals larger than 50 cm. Large eyes usually improve photon capture and the fineness with which the image is sampled; however, relatively low values of sensitivity and resolution were observed in large L. piscatorius. This indicates that a trade-off might exist between the increase in eye size as an adaptive response to the impending deep meso-and bathypelagic life and a visual constraint imposed by the quality of the water at the bottom level where contrast can be degraded by suspended particles. These results indicate that interspecific competition with sympatric and ecologically equivalent species may result in different adaptations to diurnal/nocturnal behaviour, which are sustained by morphological specialisations in sensory organs.

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The Eyes Have It: Regulatory and Structural Changes Both Underlie Cichlid Visual Pigment Diversity

Abstract: Differential gene expression and coding sequence evolution play complementary roles in the adaptive diversification of cichlid sensory systems.

Cited by 158 publications

References 66 publications

Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes

Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes

The evolution of opsins and color vision: connecting genotype to a complex phenotype

Sensory constraints in temporal segregation in two species of anglerfish, Lophius budegassa and L. piscatorius

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