Abstract
Vertebrates rely on two special groups of photoreceptor cells (rods and cones) in the retina to receive visual information. Five opsin families in the outer segment of cone cells endow fishes with color vision. Fishes encounter diverse light environments in water (various light wavelengths and intensities), so they have evolved differing numbers and amino acid compositions of cone opsin genes and, in some, phenotypic plasticity in their expression profiles to quickly adjust to new light environments. However, clear evidence for a correlation between phenotypic plasticity in cone opsin expression and adaptation is lacking. The Western mosquitofish is a highly invasive species that colonizes diverse habitats. Here, by quantifying cone opsin expression levels of individuals experiencing distinct light conditions at different developmental stages, I show that the cone opsin expression profile of juvenile and adult Western mosquitofish can quickly react to altered photic properties. Moreover, a predation experiment also demonstrates that Western mosquitofish can maintain foraging efficiency under distinct light environments. Thus, phenotypic plasticity in cone opsin expression profiles may represent a crucial trait by which Western mosquitofish successfully colonize such a wide range of aquatic habitats.
Similar content being viewed by others
References
Abrahams, M. V., D. K. Bassett & J. C. Montgomery, 2017. Sensory biology as a risk factor for invasion success and native fish decline. Transactions of the American Fisheries Society 146: 1238–1244.
Cano-Rocabayera, O., S. Vargas-Amengual, C. Aranda & A. d. Sostoa & A. Maceda-Veiga, 2020. Mosquito larvae consumption in turbid waters: the role of the type of turbidity and the larval stage in native and invasive fish. Hydrobiologia 847: 1371–1381.
Chang, C.-H., J. Catchen, R. L. Moran, A. G. Rivera-Colón, Y.-C. Wang & R. C. Fuller, 2021. Sequence analysis and ontogenetic expression patterns of cone opsin genes in the bluefin killifish (Lucania goodei). Journal of Heredity 112: 357–366.
Chang, C.-H., C.-C. Chiao & H. Y. Yan, 2009. Ontogenetic changes in color vision in the milkfish (Chanos chanos Forsskål, 1775). Zoological Science 26: 349–355.
Chang, C.-H., Y.-C. Wang, D.-C. Lee, H.-C. Yang & S.-H. Liu, 2019. Mitochondrial DNA authenticates Gambusia affinis (Baird and Girard, 1853) as the invasive mosquitofish in Taiwan. BioInvasions Records 8: 933–941.
Chang, C.-H., Y.-C. Wang, Y. T. Shao & S.-H. Liu, 2020. Phylogenetic analysis and ontogenetic changes in the cone opsins of the western mosquitofish (Gambusia affinis). PLoS ONE 15: e0240313.
Chang, C.-H. & H. Y. Yan, 2019. Plasticity of opsin gene expression in the adult red shiner (Cyprinella lutrensis) in response to turbid habitats. PLoS One 14: e0215376.
Chapman, B. B., L. J. Morrell, C. R. Tosh & J. Krause, 2010. Behavioural consequences of sensory plasticity in guppies. Proceedings of the Royal Society b: Biological Science 277: 1395–1401.
Cheng, C. L. & I. N. Flamarique, 2004. Opsin expression: new mechanism for modulating colour vision. Nature 428: 279.
Cortesi, F., Z. Musilová, S. M. Stieb, N. S. Hart, U. E. Siebeck, M. Malmstrøm, O. K. Tørresen, S. Jentoft, K. L. Cheney, N. J. Marshall, K. L. Carleton & W. Salzburger, 2015. Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes. Proceedings of the National Academy of Sciences 112: 1493–1498.
Cronin, T. W., S. Johnsen, N. J. Marshall & E. J. Warrant, 2014. Visual Ecology, Princeton University Press, Princeton, New Jersey:
Dalton, B. E. & F. d. Busserolles, N. J. Marshall & K. L. Carleton, 2017. Retinal specialization through spatially varying cell densities and opsin coexpression in cichlid fish. Journal of Experimental Biology 220: 266–277.
Dalton, B. E., E. R. Loew, T. W. Cronin & K. L. Carleton, 2014. Spectral tuning by opsin coexpression in retinal regions that view different parts of the visual field. Proceedings of the Royal Society b: Biological Science 281: 20141980.
Ehlman, S. M., B. A. Sandkam, F. Breden & A. Sih, 2015. Developmental plasticity in vision and behavior may help guppies overcome increased turbidity. Journal of Comparative Physiology A 201: 1125–1135.
Escobar-Camacho, D., E. Ramos, C. Martins & K. L. Carleton, 2017. The opsin genes of amazonian cichlids. Molecular Ecology 26: 1343–1356.
Escobar-Camacho, D., K. L. Carleton, D. W. Narain & M. E. R. Pierotti, 2020. Visual pigment evolution in Characiformes: the dynamic interplay of teleost whole-genome duplication, surviving opsins and spectral tuning. Molecular Ecology 29: 2234–2253.
Fabrin, T. M. C., L. S. Gasques, Rodrigo Junio, S. M. A. P. da Graça, W. J. Prioli & d. Graça & A. J. Prioli, 2021. Positive selection of the long-wavelength opsin gene in South American cichlid fishes. Hydrobiologia 848: 3805–3815.
Flamarique, I. N., 2013. Opsin switch reveals function of the ultraviolet cone in fish foraging. Proceedings of the Royal Society b: Biological Science 280: 20122490.
Flamarique, I. N., 2016. Diminished foraging performance of a mutant zebrafish with reduced population of ultraviolet cones. Proceedings of the Royal Society b: Biological Science 283: 20160058.
Friesen, C. N., M. E. Ramsey & M. E. Cummings, 2017. Differential sensitivity to estrogen-induced opsin expression in two poeciliid freshwater fish species. General and Comparative Endocrinology 246: 200–210.
Fryxell, D. C., E. R. Moffett, M. T. Kinnison, K. S. Simon & E. P. Palkovacs, 2022. From southern swamps to cosmopolitan model: humanity’s unfinished history with mosquitofish. Fish and Fisheries 23: 143–161.
Fuller, R. C., K. L. Carleton, J. M. Fadool, T. C. Spady & J. Travis, 2004. Population variation in opsin expression in the bluefin killifish, Lucania goodei: a real-time PCR study. Journal of Comparative Physiology A 190: 147–154.
Fuller, R. C., K. L. Carleton, J. M. Fadool, T. C. Spady & J. Travis, 2005. Genetic and environmental variation in the visual properties of bluefin killifish, Lucania goodei. Journal Evolutionay Biology 18: 516–523.
Fuller, R. C. & K. M. Claricoates, 2011. Rapid light-induced shifts in opsin expression: finding new opsins, discerning mechanisms of change, and implications for visual sensitivity. Molecular Ecology 20: 3321–3335.
Härer, A., N. Karagic, A. Meyer & J. Torres-Dowdall, 2019. Reverting ontogeny: rapid phenotypic plasticity of colour vision in cichlid fish. Royal Society Open Science 6: 190841.
Härer, A., J. Torres-Dowdall & A. Meyer, 2017. Rapid adaptation to a novel light environment: the importance of ontogeny and phenotypic plasticity in shaping the visual system of Nicaraguan Midas cichlid fish (Amphilophus citrinellus spp.). Molecular Ecology 26: 5582–5593.
Harrison, X. A., 2014. Using observation-level random effects to model overdispersion in count data in ecology and evolution. PeerJ 2: e616.
Hauser, F. E. & B. S. Chang, 2017. Insights into visual pigment adaptation and diversity from model ecological and evolutionary systems. Current Opinion Genetics & Development 47: 110–120.
Hauser, F. E., K. L. Ilves, R. K. Schott, E. Alvi, H. López-Fernández & B. S. W. Chang, 2021. Evolution, inactivation and loss of short wavelength-sensitive opsin genes during the diversification of Neotropical cichlids. Molecular Ecology 30: 1688–1703.
Hofmann, C. M., N. J. Marshall, K. Abdilleh, Z. Patel, U. E. Siebeck & K. L. Carleton, 2012. Opsin evolution in damselfish: convergence, reversal, and parallel evolution across tuning sites. Journal of Molecular Evolution 75: 79–91.
Johnsen, S. & E. A. Widder, 2001. Ultraviolet absorption in transparent zooplankton and its implications for depth distribution and visual predation. Marine Biology 138: 717–730.
Kasagi, S., K. Mizusawa & A. Takahashi, 2018. Green-shifting of SWS2A opsin sensitivity and loss of function of RH2-A opsin in flounders, genus Verasper. Ecology and Evolution 8: 1399–1410.
Kimbell, H. S., B. B. Chapman, K. E. Dobbinson & L. J. Morrell, 2019. Foraging guppies can compensate for low-light conditions, but not via a sensory switch. Behavioural Ecology and Sociobiology 73: 32.
Kirk, J. T. O., 1977a. Attenuation of light in natural waters. Australian Journal of Marine and Freshwater Research 28: 497–508.
Kirk, J. T. O., 1977b. Use of a quanta meter to measure attenuation and underwater reflectance of photosynthetically active radiation in some inland and coastal south-eastern Australian waters. Australian Journal of Marine and Freshwater Research 28: 9–21.
Kodama, I., A. Yamanaka, K. Endo & Y. Koya, 2008. Role of the yellow spot around the urogenital opening of female mosquitofish (Gambusia affinis) as a cue for copulation. Zoological Science 25: 1199–1204.
Kranz, A. M., L. G. Forgan, G. L. Cole & J. A. Rndler, 2018. Light environment change induces differential expression of guppy opsins in a muti-generational evolution experiment. Evolution 72: 1656–1676.
Langerhans, R. B., C. A. Layman, A. M. Shokrollahi & T. J. DeWitt, 2007. Predator-driven phenotypic diversification in Gambusia affinis. Evolution 58: 2305–2318.
Laver, C. R. J. & J. S. Taylor, 2011. RT-qPCR reveals opsin gene upregulation associated with age and sex in guppies (Poecilia reticulata) - a species with color-based sexual selection and 11 visual-opsin genes. BMC Evolutionary Biology 11: 81.
Lee, F., K. S. Simon & G. L. W. Perry, 2018. Prey selectivity and ontogenetic diet shift of the globally invasive western mosquitofish (Gambusia affinis) in agriculturally impacted streams. Ecology of Freshwater Fish 27: 822–833.
Leech, D. M., W. J. Boeing, S. L. Cooke, C. E. Williamson & L. Torres, 2009. UV-enhanced fish predation and the differential migration of zooplankton to UV radiation and fish. Limnology Oceanography 54: 1152–1161.
Levine, J. S. & E. F. MacNichol, 1979. Visual pigments in teleost fishes: effects of habitat, microhabitat, and behavior on visual system evolution. Sensory Processes 3: 95–135.
Lin, J.-J., F.-Y. Wang, W.-H. Li & T.-Y. Wang, 2017. The rises and falls of opsin genes in 59 ray-finned fish genomes and their implications for environmental adaptation. Scientific Reports 7: 15568.
Liu, G., Y. Cai, T. Philippi, P. Kalla, D. Scheidt, J. Richards, L. Scinto & C. Appleby, 2008. Distribution of total and methylmercury in different ecosystem compartments in the Everglades: implications for mercury bioaccumulation. Environmental Pollution 153: 257–265.
Loew, E. R. & J. N. Lythgoe, 1978. The ecology of cone pigments in teleost fishes. Vision Research 18: 715–722.
Losey, G. S., T. W. Cronin, T. H. Goldsmith, D. Hyde, N. J. Marshall & W. N. McFarland, 1999. The UV visual world of fishes: a review. Journal of Fish Biology 54: 921–943.
Luehrmann, M., S. M. Stieb, K. L. Carleton, A. Pietzker, K. L. Cheney & N. J. Marshall, 2018. Short-term colour vision plasticity on the reef: changes in opsin expression under varying light conditions differ between ecologically distinct fish species. Journal of Experimental Biology 221: 175281.
Lythgoe, J. N., 1984. Visual pigments and environmental light. Vision Research 24: 1539–1550.
Marques, D. A., J. S. Taylor, F. C. Jones, F. D. Palma, D. M. Kingsley & T. E. Reimchen, 2017. Convergent evolution of SWS2 opsin facilitates adaptive radiation of threespine stickleback into different light environments. PLoS Biology 15: e2001627.
Matsumoto, Y., S. Oda, H. Mitani & S. Kawamura, 2020. Orthologous divergence and paralogous anticonvergence in molecular evolution of triplicated green opsin genes in medaka fish, genus Oryzias. Genome Biology and Evolution 12: 911–923.
Murphy, M. J. & E. L. Westerman, 2022. Evolutionary history limits species’ ability to match colour sensitivity to available habitat light. Proceedings of the Royal Society b: Biological Science 289: 20220612.
Musilova, Z., A. Indermaur, A. R. Bitja-Nyom, D. Omelchenko, M. Kłodawska, L. Albergati, K. Remišová & W. Salzburger, 2019. Evolution of the visual sensory system in cichlid fishes from crater lake Barombi Mbo in Cameroon. Molecular Ecology 28: 5010–5031.
Musilova, Z., W. Salzburger & F. Cortesi, 2021. The visual opsin gene repertoires of teleost fishes: evolution, ecology, and function. Annual Review of Cell and Developmental Biology 37: 1–28.
Musser, J. M. & D. Arendt, 2017. Loss and gain of cone types in vertebrate ciliary photoreceptor evolution. Developmental Biology 431: 26–35.
Nandamuri, S. P., M. R. Yourick & K. L. Carleton, 2017. Adult plasticity in African cichlids: rapid changes in opsin expression in response to environmental light differences. Molecular Ecology 26: 6036–6052.
Nettle, D. & M. Bateson, 2015. Adaptive developmental plasticity: what is it, how can we recognize it and when can it evolve. Proceedings of the Royal Society b: Biological Science 282: 20151005.
Orger, M. B. & H. Baier, 2005. Channeling of red and green cone inputs to the zebrafish optomotor response. Visual Neuroscience 22: 275–281.
Pohlmann, K., J. Atema & T. Breithaupt, 2004. The importance of the lateral line in nocturnal predation of piscivorous catfish. Journal of Experimental Biology 207: 2971–2978.
Pohlmann, K., F. W. Grasso & T. Breithaupt, 2001. Tracking wakes: the nocturnal predatory strategy of piscivorous catfish. Proceedings of the National Academy of Sciences 98: 7371–7374.
Polverino, G., J. C. Liao & M. Porfiri, 2013. Mosquitofish (Gambusia affinis) preference and behavioral response to animated images of conspecifics altered in their color, aspect ratio, and swimming depth. PLoS ONE 8: e54315.
Pyke, G. H., 2005. A review of the biology of Gambusia affinis and G. holbrooki. Reviews in Fish Biology and Fisheries 15: 339–365.
Rajasekharan, P. T. & B. N. Chowdaiah, 1972. Selective feeding behaviour of Gambusia affinis. Oecologia 11: 79–81.
Reddy, S. R. & G. Kote, 1975. Predatory behavior of Gambusia affinis in relation to different light colors. Physiology and Behavior 14: 255–257.
Rennison, D. J., G. L. Owens, N. Heckman, D. Schluter & T. Veen, 2016. Rapid adaptive evolution of colour vision in the threespine stickleback radiation. Proceedings of the Royal Society b: Biological Science 283: 20160242.
Rodríguez, C. F., E. Bécares & M. Fernández-Aláez, 2003. Shift from clear to turbid phase in Lake Chozas (NW Spain) due to the introduction of American red swamp crayfish (Procambarus clarkii). Hydrobiologia 506: 421–426.
Ruehl, C. B. & T. J. DeWitt, 2005. Trophic plasticity and fine-grained resource variation in populations of western mosquitofish, Gambusia affinis. Evolutionary Ecology Research 7: 801–819.
Russo, G., A. Chou, J. E. Rettig & G. R. Smith, 2008. Foraging responses of mosquitofish (Gambusia affinis) to Items of different sizes and colors. Journal of Freshwater Ecology 23: 677–678.
Sabbah, S., J. Hui, F. E. Hauser, W. A. Nelson & C. W. Hawryshyn, 2012. Ontogeny in the visual system of Nile tilapia. Journal of Experimental Biology 215: 2684–2695.
Sakai, Y., H. Ohtsuki, S. Kasagi, S. Kawamura & M. Kawata, 2016. Effects of light environment during growth on the expression of cone opsin genes and behavioral spectral sensitivities in guppies (Poecilia reticulata). BMC Evolutionary Biology 16: 106.
Sakai, Y., S. Kawamura & M. Kawata, 2018. Genetic and plastic variation in opsin gene expression, light sensitivity, and female response to visual signals in the guppy. Proceedings of the National Academy of Sciences 115: 12247–12252.
Sandkam, B., B. Dalton, F. Breden & K. Carleton, 2018. Reviewing guppy color vision: integrating the molecular and physiological variation in visual tuning of a classic system for sensory drive. Current Zoology 64: 535–545.
Seehausen, O., 2015. Beauty varies with the light. Nature 521: 34–35.
Seehausen, O., Y. Terai, I. S. Magalhaes, K. L. Carleton, H. D. J. Mrosso, R. Miyagi, I. van der Sluijs, M. V. Schneider, M. E. Maan, H. Tachida, H. Imai & N. Okada, 2008. Speciation through sensory drive in cichlid fish. Nature 455: 620–626.
Shao, Y. T., F.-Y. Wang, W.-C. Fu, H. Y. Yan, K. Anraku, I.-S. Chen & B. Borg, 2014. Androgens increase lws opsin expression and red sensitivity in male three-spined sticklebacks. PLoS ONE 9: e100330.
Sibeaux, A., M. L. Keser, G. L. Cole, A. M. Kranz & J. A. Endler, 2019. How viewing objects with the dorsal or ventral retina affects colour-related behaviour in guppies (Poecilia reticulata). Vision Research 158: 78–89.
Smith, A. R., L. D’annunzio, A. E. Smith, A. Sharma, C. M. Hofmann, N. J. Marsall & K. L. Carleton, 2011. Intraspecific cone opsin expression variation in the cichlids of Lake Malawi. Molecular Ecology 20: 299–310.
Smith, A. R., K. Ma, D. Soares & K. L. Carleton, 2012. Relative LWS cone opsin expression determines optomotor thresholds in Malawi cichlid fish. Genes, Brain and Behavior 11: 185–192.
Snell-Rood, E. C., 2013. An overview of the evolutionary causes and consequences of behavioural plasticity. Animal Behaviour 85: 1004–1011.
Stieb, S. M., K. L. Chareton, F. Cortesi, N. J. Marshall & W. Salzburger, 2016. Depth-dependent plasticity in opsin gene expression varies between damselfish (Pomacentridae) species. Molecular Ecology 25: 3645–3661.
Stockwell, C. A. & S. C. Weeks, 1999. Translocations and rapid evolutionary responses in recently established populations of western mosquitofish (Gambusia affinis). Animal Conservation 2: 103–110.
Tałanda, J., P. Maszczyk & E. Babkiewicz, 2018. The reaction distance of a planktivorous fish (Scardinius erythrophthalmus) and the evasiveness of its prey (Daphnia pulex × pulicaria) under different artificial light spectra. Limnology 19: 311–319.
Tobler, M., S. W. Coleman, B. D. Perkins & G. G. Rosenthal, 2010. Reduced opsin gene expression in a cave-dwelling fish. Biology Letters 6: 98–101.
Torres-Dowdall, J., N. Karagic, A. Härer & A. Meyer, 2021. Diversity in visual sensitivity across Neotropical cichlid fishes via differential expression and intraretinal variation of opsin genes. Molecular Ecology 30: 1880–1891.
Tsurui-Sato, K., S. Fujimoto, O. Deki, T. Suzuki, H. Tatsuta & K. Tsuji, 2019. Reproductive interference in live-bearing fish: the male guppy is a potential biological agent for eradicating invasive mosquitofish. Scientific Reports 9: 5439.
Veen, T., C. Brock, D. Rennison & D. Bolnick, 2017. Plasticity contributes to a fine-scale depth gradient in sticklebacks’ visual system. Molecular Ecology 26: 4339–4350.
Watson, C. T., S. M. Gray, M. Hoffmann, K. P. Lubieniecki, J. B. Joy, B. A. Sandkam, D. Weigel, E. Loew, C. Dreyer, W. S. Davidson & F. Breden, 2011. Gene duplication and divergence of long wavelength-sensitive opsin genes in the guppy, Poecilia reticulata. Journal of Molecular Evolution 72: 240–322.
Watson, C. T., K. P. Lubieniecki, E. Loew, W. S. Davidson & F. Breden, 2010. Genomic organization of duplicated short wave-sensitive and long wave-sensitive opsin genes in the green swordtail, Xiphophorus helleri. BMC Evolutionary Biology 10: 87.
Wright, D. S. & R. v. Eijk, L. Schuart, O. Seehausen, T. G. G. Groothuis & M. E. Maan, 2020. Testing sensory drive speciation in cichlid fish: linking light conditions to opsin expression, opsin genotype and female mate preference. Journal of Evolutionary Biology 33: 422–434.
Yokoyama, S., 2000. Molecular evolution of vertebrate visual pigments. Progress in Retinal and Eye Research 19: 385–491.
Yoshimatsu, T., C. Schröder, N. E. Nevala, P. Berens & T. Baden, 2020. Fovea-like photoreceptor specializations underlie single UV cone driven prey-capture behavior in zebrafish. Neuron 107: 320-337.e6.
Zukoshia, R., I. Savellia & I. N. Flamarique, 2018. Foraging performance of two fishes, the threespine stickleback and the Cumaná guppy, under different light backgrounds. Vision Research 145: 31–38.
Acknowledgements
The author was supported by grants from the Ministry of Science and Technology, Taiwan (MOST 110-2621-B-029-005, 110-2621-B-152-001, 111-2621-B52-001-MY2). Dr. Yi Ta Shao at the Institute of Marine Biology (National Taiwan Ocean University) and Dr. Yung-Che Tseng at the Institute of Cellular and Organismic Biology (Academia Sinica) provided technical assistance. Mr. Chih-Chiang Lee and Ms. Ting-Ting Huang helped take care of the experimental animals and in collecting experimental data. Dr. John O’Brien provided editing assistance.
Author information
Authors and Affiliations
Contributions
C-HC conceived the project, was responsible for experimental animal care, data collection and analysis, and prepared the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The author declares that he has no competing interests.
Additional information
Handling editor: Cécile Fauvelot
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Chang, CH. Rapid adjustment of cone opsin expression profiles may help Western mosquitofish (Gambusia affinis) maintain foraging efficiency in distinct light environments. Hydrobiologia 850, 1059–1071 (2023). https://doi.org/10.1007/s10750-023-05139-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-023-05139-0