Abstract
Evolution of male-biased coloration in the guppy Poecilia reticulata is driven by sexual and natural selection. The colorful male ornaments are attractive to females, but also attract predators. Distinct predation regimes in Trinidadian streams promote the evolution of different guppy color morphs, with male ornamentation and female mate preference also co-evolving among populations. How attractive a male guppy color morph is to a female depends not only on the coloration itself, but also on how strongly the morph evokes stimulation of the female visual system. Both allele type and gene expression levels of cone opsin genes play a role in female mate preferences. Previous studies have demonstrated that predation can alter female guppy mate choice, but the underlying mechanism remains unclear. Here, I hypothesize that guppies adjust their cone opsin expression profiles in response to predation pressure. Although I detected a significant change in LWS-R transcription in response to predation, cone opsin expression profiles in adult female guppies do not appear to be driven by predation pressure. However, the impacts of predation pressure on developmental plasticity in cone opsin expression and brain anatomy remain promising avenues of further investigation to determine how predators affect female mate preference in guppies.
Similar content being viewed by others
References
Aramaki M, Wu X, Liu H, Liu Y, Cho Y-W, Song M, Fu Y, Ng L, Forrest D (2022) Transcriptional control of cone photoreceptor diversity by a thyroid hormone receptor. Proc Natl Acad Sci U S A 119:e2209884119
Balasch JC, Tort L (2019) Netting the stress responses in fish. Front Endocrinol 12:62
Balleine BW (2007) The neural basis of choice and decision making. J Neurosci 27:8159–8160
Bolstad K, Flamarique IN (2023) Two mechanisms of retinal photoreceptor plasticity underlie rapid adaptation to novel light environments. J Comp Neurol 531:1080–1094
Briggs SE, Godin J-GJ, Dugatkin LA (1996) Mate-choice copying under predation risk in the Trinigadian guppy (Poecilia reticulata). Behav Ecol 7:151–157
Butler JM, Maruska KP (2021) Opsin expression varies with reproductive state in the cichlid fish Astatotilapia burtoni. Integr Comp Biol 61:240–248
Chang C-H (2022) Correlated expression of the opsin retrogene LWS-R and its host gene in two poeciliid fishes. Zool Stud 61:16
Chang C-H (2023) Rapid adjustment of cone opsin expression profiles may help Western mosquitofish (Gambusia affinis) maintain foraging efficiency in distinct light environments. Hydrobiologia 850:1059–1071
Chang C-H, Yan HY (2019) Plasticity of opsin gene expression in the adult red shiner (Cyprinella lutrensis) in response to turbid habitats. PLoS One 14:e0215376
Chang C-H, Chiao C-C, Yan HY (2009) Ontogenetic changes in color vision in the milkfish (Chanos chanos Forsskål, 1775). Zoolog Sci 26:349–355
Chang C-H, Wang Y-C, Shao YT, Liu S-H (2020) Phylogenetic analysis and ontogenetic changes in the cone opsins of the western mosquitofish (Gambusia affinis). PLoS One 15:e0240313
Chang C-H, Catchen J, Moran RL, Rivera-Colón AG, Wang Y-C, Fuller RC (2021) Sequence analysis and ontogenetic expression patterns of cone opsin genes in the bluefin killifish (Lucania goodei). J Hered 112:357–366
Cheng CL, Flamarique IN (2004) Opsin expression: new mechanism for modulating colour vision. Nature 428:279
Cheng CL, Gan KJ, Flamarique IN (2009) Thyroid hormone induces a time-dependent opsin switch in the retina of salmonid fishes. Invest Ophthalmol Vis Sci 50:3024–3032
Cocco A, Rönnberg AMC, Jin Z, André GI, Vossen LE, Bhandage AK, Thörnqvist P-O, Birnir B, Winberg S (2017) Characterization of the γ-aminobutyric acid signaling system in the zebrafish (Danio rerio Hamilton) central nervous system by reverse transcription-quantitative polymerase chain reaction. Neuroscience 343:300–321
Cole GL, Endler JA (2015) Variable environmental effects on a multicomponent sexually selected trait. Am Nat 185:452–468
Corral-López A, Bloch NI, Kotrschal A, van der Bijl W, Buechel SD, Mank JE, Kolm N (2017) Female brain size affects the assessment of male attractiveness during mate choice. Sci Adv 3:e1601990
Cortesi F, Musilová Z, Stieb SM, Hart NS, Siebeck UE, Malmstrøm M, Tørresen OK, Jentoft S, Cheney KL, Marshall NJ, Carleton KL, Salzburger W (2015) Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes. Proc Natl Acad Sci U S A 112:1493–1498
Cronin TW, Johnsen S, Marshall NJ, Warrant EJ (2014) Visual Ecology. Princeton University Press, Princeton, New Jersey
Cuthill IC, Allen WL, Arbuckle K, Caspers B, Chaplin G, Hauber ME, Hill GE, Jablonski NG, Jiggins CD, Kelber A, Mappes J, Marshall J, Merrill R, Osorio D, Prum R, Roberts NW, Roulin A, Rowland HM, Sherratt TN, Skelhorn J, Speed MP, Stevens M, Stoddard MC, Stuart-Fox D, Talas L, Tibbetts E, Caro T (2017) The biology of color. Science 357:eaan0221
Dzikowski R, Hulata G, Harpaz S, Karplus I (2004) Inducible reproductive plasticity of the guppy Poecilia reticulata in response to predation cues. J Exp Zool A Comp Exp Biol 301A:776–782
Ehlman SM, Sandkam BA, Breden F, Sih A (2015) Developmental plasticity in vision and behavior may help guppies overcome increased turbidity. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 201:1125–1135
Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91
Evans JP, Kelley JL, Ramnarine IW, Pilastro A (2002) Female behaviour mediates male courtship under predation risk in the guppy (Poecilia reticulata). Behav Ecol Sociobiol 52:469–502
Evans JP, Gasparini C, Pilastro A (2007) Female guppies shorten brood retention in response to predator cues. Behav Ecol Sociobiol 61:719–727
Farre A, Mackin R, Stenkamp DL (2019) Thyroid hormone regulates the tandemly-quadruplicated rh2 cone opsin gene array in zebrafish. Invest Ophthalmol Vis Sci 60:6039
Fischer EK, Harris RM, Hofmann HA, Hoke KL (2014) Predator exposure alters stress physiology in guppies across timescales. Horm Behav 65:165–172
Flamarique IN, Ahmed AS, Cheng CL, Molday RS, Devlin RH (2019) Growth hormone regulates opsin expression in the retina of a salmonid fish. J Neuroendocrinol 31:e12804
Friesen CN, Ramsey ME, Cummings ME (2017) Differential sensitivity to estrogen-induced opsin expression in two poeciliid freshwater fish species. Gen Comp Endocrinol 246:200–210
Fuller RC, Claricoates KM (2011) Rapid light-induced shifts in opsin expression: finding new opsins, discerning mechanisms of change, and implications for visual sensitivity. Mol Ecol 20:3321–3335
Fuller RC, Noa LA, Strellner RS (2010) Teasing apart the many effects of lighting environment on opsin expression and foraging preference in bluefin killifish. Am Nat 176:1–13
Glavaschi A, Cattelan S, Devigili A, Pilastro A (2022) Immediate predation risk alters the relationship between potential and realised selection on male traits in the Trinidad guppy Poecilia reticulata. Proc R Soc B 289:20220641
Godin J-GJ, Briggs SE (1996) Female mate choice under predation risk in the guppy. Anim Behav 51:117–130
Godin J-GJ, McDonough HE (2003) Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait. Behav Ecol 14:194–200
Goikoetxea A, Todd EV, Gemmell NJ (2017) Stress and sex: does cortisol mediate sex change in fish? Reproduction 154:R149–R160
Gong A, Gibson RM (1996) Reversal of a female preference after visual exposure to a predator in the guppy, Poecilia reticulata. Anim Behav 52:1007–1015
Gordon SP, Hendry AP, Reznick DN (2017) Predator-induced contemporary evolution, phenotypic plasticity, and the evolution of reaction norms in guppies. Copeia 105:514–522
Gosline AK, Rodd FH (2008) Predator-induced plasticity in guppy (Poecilia reticulata) life history traits. Aquat Ecol 42:693–699
Handelsman CA, Broder ED, Dalton CM, Ruell EW, Myrick CA, Reznick DN, Ghalambor CK (2013) Predator-Induced phenotypic plasticity in metabolism and rate of growth: rapid adaptation to a novel environment. Integr Comp Biol 53:975–988
Härer A, Torres‐Dowdall J, Meyer A (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.). Mol Ecol 26:5582–5593
Härer A, Karagic N, Meyer A, Torres-Dowdall J (2019) Reverting ontogeny: rapid phenotypic plasticity of colour vision in cichlid fish. R Soc Open Sci 6:190841
Hauser FE, Chang BS (2017) Insights into visual pigment adaptation and diversity from model ecological and evolutionary systems. Curr Opin Genet Dev 47:110–120
Hofmann CM, O'quin KE, Smith AR, Carleton KL (2010) Plasticity of opsin gene expression in cichlids from Lake Malawi. Mol Ecol 19:2064–2074
Kanazawa N, Goto M, Harada Y, Takimoto C, Sasaki Y, Uchikawa T, Kamei Y, Matsuo M, Fukamachi S (2020) Changes in a cone opsin repertoire affect color-dependent social behavior in medaka but not behavioral photosensitivity. Front Genet 11:801
Karagic N, Härer A, Meyer A, Torres-Dowdall J (2022) Thyroid hormone tinkering elicits integrated phenotypic changes potentially explaining rapid adaptation of color vision in cichlid fish. Evolution 76:837–845
Kawamoto M, Ishii Y, Kawata M (2021) Genetic basis of orange spot formation in the guppy (Poecilia reticulata). BMC Ecol Evol 21:211
Kawamura S, Kasagi S, Kasai D, Tezuka A, Shoji A, Takahashi A, Imai H, Kawata M (2016) Spectral sensitivity of guppy visual pigments reconstituted in vitro to resolve association of opsins with cone cell types. Vision Res 127:67–73
Kemp DJ, Reznick DN, Grether GF, Endler JA (2009) Predicting the direction of ornament evolution in Trinidadian guppies (Poecilia reticulata). Proc R Soc B 27:64335–64343
Koch RE, Hill GE (2018) Do carotenoid-based ornaments entail resource trade-offs? An evaluation of theory and data. Funct Ecol 32:1908–1920
Kotrschal A, Buechel SD, Zala SM, Corral-Lopez A, Penn DJ, Kolm N (2015) Brain size affects female but not male survival under predation threat. Ecol Lett 18:646–652
Kotrschal A, Deacon AE, Magurran AE, Kolm N (2017) Predation pressure shapes brain anatomy in the wild. Evol Ecol 31:619–633
Kranz AM, Forgan LG, Cole GL, Endler JA (2018) Light environment change induces differential expression of guppy opsins in a multi‐generational evolution experiment. Evolution 72:1656–1676
Land MF, Nisson D-E (2012) Animal eyes. Oxford University Press, Oxford
Laver CRJ, Taylor JS (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 Evol Biol 11:81
Li L-C, Roufidou C, Borg B, Shao YT (2022) Changes in red color sensitivity over the spawning cycle of female three-spined stickleback (Gasterosteus aculeatus). Zool Stud 61:17
Lin J-J, Wang F-Y, Li W-H, Wang T-Y (2017) The rises and falls of opsin genes in 59 ray-finned fish genomes and their implications for environmental adaptation. Sci Rep 7:15568
Luehrmann M, Stieb SM, Carleton KL, Pietzker A, Cheney KL, Marshall NJ (2018) Short-term colour vision plasticity on the reef: changes in opsin expression under varying light conditions differ between ecologically distinct fish species. J Exp Biol 221:jeb175281
Magurran AE (1998) Population differentiation without speciation. Philos Trans R Soc Lond B Biol Sci 353:275–286
Magurran AE (2005) Evolutionary ecology: the Trinidadian Guppy. Oxford University Press, Oxford
Mitchell DJ, Vega-Trejo R, Kotrschal A (2020) Experimental translocations to low predation lead to non-parallel increases in relative brain size. Biol Lett 16:20190654
Nandamuri SP, Yourick MR, Carleton KL (2017) Adult plasticity in African cichlids: rapid changes in opsin expression in response to environmental light differences. Mol Ecol 26:6036–6052
Nandamuri SP, Schulte JE, Yourick MR, Sandkam BA, Behrens KA, Schreiner MM, Dayanim M, Sweatt G, Conte MA, Juntti SA, Carleton KL (2023) A second locus contributing to the differential expression of the blue sensitive opsin SWS2A in Lake Malawi cichlids. Hydrobiologia 850:2331–2353
Nordell SE (1998) The response of female guppies, Poecilia reticulata, to chemical stimuli from injured conspecifics. Environ Biol Fishes 51:331–338
Ord J, Holmes KE, Holt WV, Fazeli A, Watt PJ (2020) Premature birth stunts early growth and is a possible driver of stress-induced maternal effects in the guppy Poecilia reticulata. J Fish Biol 96:506–515
Peter MCS (2011) The role of thyroid hormones in stress response of fish. Gen Comp Endocrinol 172:198–210
Prazdnikov DV (2021) Role of thyroid hormones in color diversity of male guppies: experimental data on Endler’s guppy (Poecilia wingei). Environ Biol Fishes 104:675–688
Reddon AR, Chouinard-Thuly L, Leris I, Reader SM (2018) Wild and laboratory exposure to cues of predation risk increases relative brain mass in male guppies. Funct Ecol 32:1847–1856
Reyes AS, Bittar A, Ávila LC, Botia C, Esmeral NP, Bloc NI (2022) Divergence in brain size and brain region volumes across wild guppy populations. Proc R Soc B 289:20212784
Ruell EW, Handelsman CA, Hawkins CL, Sofaer HR, Ghalambor CK, Angeloni L (2013) Fear, food and sexual ornamentation: plasticity of colour development in Trinidadian guppies. Proc R Soc B 280:20122019
Sakai Y, Ohtsuki H, Kasagi S, Kawamura S, Kawata M (2016) Effects of light environment during growth on the expression of cone opsin genes and behavioral spectral sensitivities in guppies (Poecilia reticulata). BMC Evol Biol 16:106
Sakai Y, Kawamura S, Kawata M (2018) Genetic and plastic variation in opsin gene expression, light sensitivity, and female response to visual signals in the guppy. Proc Natl Acad Sci U S A 115:12247–12252
Sandkam B, Young CM, Breden F (2015) Beauty in the eyes of the beholders: colour vision is tuned to mate preference in the Trinidadian guppy (Poecilia reticulata). Mol Ecol 24:596–609
Sandkam BA, Young CM, Breden FMW, Bourne GR, Breden F (2015) Color vision varies more among populations than among species of live-bearing fish from South America. BMC Evol Biol 15:225
Sandkam B, Dalton B, Breden F, Carleton K (2018) Reviewing guppy color vision: integrating the molecular and physiological variation in visual tuning of a classic system for sensory drive. Curr Zool 64:535–545
Sandkam BA, Campello L, O’Brien C, Nandamuri SP, Gammerdinger WJ, Conte MA, Swaroop A, Carleton KL (2020) Tbx2a modulates switching of RH2 and LWS opsin gene expression. Mol Biol Evol 37:2002–2014
Schreiner MM, Yourick MR, Juntti SA, Carleton KL (2022) Environmental plasticity in opsin expression due to light and thyroid hormone in adult and developing Astatotilapia burtoni. Hydrobiologia 850:2315–2329
Schwartz AK, Hendry AP (2007) A test for the parallel co-evolution of male colour and female preference in Trinidadian guppies (Poecilia reticulata). Evol Ecol Res 9:71–90
Seehausen O (2015) Beauty varies with the light. Nature 521:34–35
Shao YT, Wang F-Y, Fu W-C, Yan HY, Anraku K, Chen I-S, Borg B (2014) Androgens increase lws opsin expression and red sensitivity in male three-spined sticklebacks. PLoS One 9:e100330
Sommer RJ (2020) Phenotypic plasticity: from theory and genetics to current and future challenges. Genetics 215:1–13
Stieb SM, Chareton KL, Cortesi F, Marshall NJ, Salzburger W (2016) Depth-dependent plasticity in opsin gene expression varies between damselfish (Pomacentridae) species. Mol Ecol 25:3645–3661
Striedter GF (2005) Principles of brain evolution. Sinauer Associates is an imprint of Oxford University Press, Massachusetts
Tsujimura T (2020) Mechanistic insights into the evolution of the differential expression of tandemly arrayed cone opsin genes in zebrafish. Dev Growth Differ 62:465–475
Vega-Trejo R, Vila-Pouca C, Mitchell DJ, Kotrschal A (2022) Predation impacts brain allometry in female guppies (Poecilia reticulata). Evol Ecol 36:1045–1059
Volkov LI, Kim-Han JS, Saunders LM, Poria D, Hughes AEO, Kefalov VJ, Parichy DM, Corbo JC (2020) Thyroid hormone receptors mediate two distinct mechanisms of long-wavelength vision. Proc Natl Acad Sci U S A 117:15262–15269
Ward MN, Churcher AM, Dick KJ, Laver CRJ, Owens GL, Polack MD, Ward PR, Breden F, Taylor JS (2008) The molecular basis of color vision in colorful fish: four long wave-sensitive (LWS) opsins in guppies (Poecilia reticulata) are defined by amino acid substitutions at key functional sites. BMC Evol Biol 8:210
Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385–491
Acknowledgments
The author was supported by grants from the National Science and Technology Council, Taiwan (MOST 111-2621-B-029-003-MY2). The author thanks Dr. Yi Ta Shao, Dr. Yung-Che Tseng, and Mr. Pou-Long Kuan for offering technical assistance, and Mr. Chia-Yen Lin for illustrating Fig. 1. Dr. John O’Brien provided English editing assistance.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that he has no competing interests.
Ethic approval
No formal ethics approval was required for the study; however, the experiment was approved by the Institutional Animal Care and Use Committee (IACUC) at Tunghai University, Taiwan.
Additional information
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.
About this article
Cite this article
Chang, CH. Does predation pressure alter the visual properties of prey? An assessment of the guppy Poecilia reticulata. Ichthyol Res (2024). https://doi.org/10.1007/s10228-024-00957-1
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10228-024-00957-1