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Enhanced ambient UVB radiation affects post-mating, but not pre-mating sexual traits in a fish

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Organisms inhabiting shallow aquatic habitats currently experience increasing levels of solar ultraviolet B radiation (UVB). UVB causes damage on cellular and molecular levels and can affect associated life-history traits either through direct exposure or indirectly through oxidative stress generation. We examined UVB effects on pre- and post-mating sexual traits in three-spined stickleback fish (Gasterosteus aculeatus). Adult, reproductively non-active males were assigned to two exposure treatments under semi-natural conditions in an outdoor experiment; one group received natural radiation (UVBnormal) whilst the other group received additional UVB (UVBenhanced). After two months, colour metrics were used to quantify male breeding colouration as pre-mating trait. At the post-mating stage, sperm morphology, number and movement as well as testes mass were determined. Males did not significantly differ in sexual ornamentation between treatments, but UVBenhanced fish had smaller testes as well as fewer and shorter sperm than UVBnormal fish. Sperm movement was not significantly different between treatments. However, in UVBenhanced males, linear and progressive movement of sperm was positively correlated with sperm morphology (head-to-tail length ratio), whereas in UVBnormal males this relationship was negative (but not significant). Additionally, there was a significant treatment by body condition interaction concerning head-to-tail length ratio, i.e. head-to-tail length ratio increased with condition in UVBnormal males whereas there was no relationship in UVBenhanced fish. Our findings reveal that increased UVB levels influence post-mating fitness-relevant traits in males whilst having no significant impact on pre-mating sexual traits, suggesting selective UVB-effects at the gamete level with consequences for reproductive performance.

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  1. Andersson MB (1994) Sexual selection. Princeton University Press, Princeton

  2. Andrady AL, Aucamp PJ, Austin AT, Bais AF, Ballare CL, Bjorn LO, Bornman JF, Caldwell M, Cullen AP, Erickson DJ (2012) Environmental effects of ozone depletion and its interactions with climate change: progress report, 2011. Photochem Photobiol Sci 11:13–27

  3. Au DWT, Chiang MWL, Tang JYM, Yuen BBH, Wang YL, Wu RSS (2002) Impairment of sea urchin sperm quality by UV-B radiation: predicting fertilization success from sperm motility. Mar Pollut Bull 44:583–589

  4. Bais A, McKenzie R, Bernhard G, Aucamp P, Ilyas M, Madronich S, Tourpali K (2015) Ozone depletion and climate change: impacts on UV radiation. Photochem Photobiol Sci 14:19–52

  5. Bakker TCM, Milinski M (1993) The advantages of being red: sexual selection in the stickleback. Mar Behav Physiol 23:287–300

  6. Bakker TCM, Zbinden M, Frommen JG, Weiss A, Largiadèr CR (2006) Slow fertilization of stickleback eggs: the result of sexual conflict? BMC Ecol 6:7

  7. Ball WT, Alsing J, Mortlock DJ, Staehelin J, Haigh JD, Peter T, Tummon F, Stübi R, Stenke A, Anderson J (2018) Evidence for a continuous decline in lower stratospheric ozone offsetting ozone layer recovery. Atmos Chem Phys 18:1379–1394

  8. Blount JD, Pike TW (2012) Deleterious effects of light exposure on immunity and sexual coloration in birds. Funct Ecol 26:37–45

  9. Borg B (1982) Seasonal effects of photoperiod and temperature on spermatogenesis and male secondary sexual characters in the three-spined stickleback, Gasterosteus aculeatus L. Can J Zool 60:3377–3386

  10. Breckels RD, Neff BD (2013) The effects of elevated temperature on the sexual traits, immunology and survivorship of a tropical ectotherm. J Exp Biol 216:2658–2664

  11. Browman HI, Vetter RD, Rodriguez CA, Cullen JJ, Davis RF, Lynn E, St Pierre J-F (2003) Ultraviolet (280–400 nm)-induced DNA damage in the eggs and larvae of Calanus finmarchicus G. (Copepoda) and Atlantic cod (Gadus morhua). Photochem Photobiol 77:397–404

  12. Budaev SV (2010) Using principal components and factor analysis in animal behaviour research: caveats and guidelines. Ethology 116:472–480

  13. Candolin U (1998) Reproduction under predation risk and the trade-off between current and future reproduction in the threespine stickleback. Proc R Soc Lond B 265:1171–1175

  14. Carreja B, Fernández M, Agustí S (2016) Joint additive effects of temperature and UVB radiation on zoeae of the crab Taliepus dentatus. Mar Ecol Prog Ser 550:135–145

  15. Cone RS (1989) The need to reconsider the use of condition indices in fishery science. Trans Am Fish Soc 118:510–514

  16. Dahms H-U, Lee J-S (2010) UV radiation in marine ectotherms: molecular effects and responses. Aquat Toxicol 97:3–14

  17. den Outer PN, Slaper H, Tax RB (2005) UV radiation in the Netherlands: assessing long-term variability and trends in relation to ozone and clouds. J Geophys Res Atmos 110:D02203

  18. Elofsson H, Van Look KJ, Sundell K, Sundh H, Borg B (2006) Stickleback sperm saved by salt in ovarian fluid. J Exp Biol 209:4230–4237

  19. Endler JA (1983) Natural and sexual selection on color pattern in poeciliid fishes. Environ Biol Fishes 9:173–190

  20. Endler JA, Mielke PW (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc 86:405–431

  21. Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967–971

  22. Evans J, Garcia-Gonzalez F (2016) The total opportunity for sexual selection and the integration of pre- and post-mating episodes of sexual selection in a complex world. J Evol Biol 29:2338–2361

  23. Fukunishi Y, Masuda R, Yamashita Y (2006) Ontogeny of tolerance to and avoidance of ultraviolet radiation in red sea bream Pagrus major and black sea bream Acanthopagrus schlegeli. Fish Sci 72:356–363

  24. Fukunishi Y, Masuda R, Yamashita Y (2010) Exposure of eggs to solar UV-B leads to reduced hatching rates in two sparid fishes, red sea bream Pagrus major and black sea bream Acanthopagrus schlegeli. J Fish Biol 76:734–741

  25. Gomez D (2006) AVICOL, a program to analyse spectrometric data. Last updated October 2011. Free program available at http://sites.google.com/site/avicolprogram/ or from the author at dodo-gomez@yahoo.fr

  26. Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17:509–528

  27. Groff AA, da Silva J, Nunes EA, Ianistcki M, Guecheva TN, de Oliveira AM, de Oliveira CPF, Val AL, JoAP Henriques (2010) UVA/UVB-induced genotoxicity and lesion repair in Colossoma macropomum and Arapaima gigas Amazonian fish. J Photochem Photobiol B 99:93–99

  28. Grubbs FE (1969) Procedures for detecting outlying observations in samples. Technometrics 11:1–21

  29. Häder DP, Kumar HD, Smith RC, Worrest RC (1998) Effects on aquatic ecosystems. J Photochem Photobiol B 46:53–68

  30. Häder D-P, Kumar H, Smith R, Worrest R (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 6:267–285

  31. Hawkes JW (1974) The structure of fish skin. Cell Tissue Res 149:147–158

  32. Herrling T, Jung K, Fuchs J (2006) Measurements of UV-generated free radicals/reactive oxygen species (ROS) in skin. Spectrochim Acta A 63:840–845

  33. Hiermes M, Bakker TCM, Mehlis M, Rick IP (2015) Context-dependent dynamic UV signaling in female threespine sticklebacks. Sci Rep 5:17474

  34. Hiermes M, Rick IP, Mehlis M, Bakker TCM (2016) The dynamics of color signals in male threespine sticklebacks Gasterosteus aculeatus. Curr Zool 62:23–31

  35. Humphries S, Evans JP, Simmons LW (2008) Sperm competition: linking form to function. BMC Evol Biol 8:319

  36. Immler S, Pryke SR, Birkhead TR, Griffith SC (2010) Pronounced within-individual plasticity in sperm morphometry across social environments. Evolution 64:1634–1643

  37. Jakob EM, Marshall SD, Uetz GW (1996) Estimating fitness: a comparison of body condition indices. Oikos 77:61–67

  38. Jokinen EI, Salo HM, Markkula SE, Immonen AK, Aaltonen TM (2001) Ultraviolet B irradiation modulates the immune system of fish (Rutilus rutilus, Cyprinidae). Part III: lymphocytes. Photochem Photobiol 73:505–512

  39. Jokinen IE, Markkula ES, Salo HM, Kuhn P, Nikoskelainen S, Arts MT, Browman HI (2008) Exposure to increased ambient ultraviolet B radiation has negative effects on growth, condition and immune function of juvenile Atlantic salmon (Salmo salar). Photochem Photobiol 84:1265–1271

  40. Kerr J, McElroy C (1993) Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion. Science 262:1032–1034

  41. Kotiaho JS (2001) Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence. Biol Rev 76:365–376

  42. Kouwenberg J, Browman H, Cullen J, Davis R, St-Pierre J-F, Runge J (1999) Biological weighting of ultraviolet (280–400 nm) induced mortality in marine zooplankton and fish. I. Atlantic cod (Gadus morhua) eggs. Mar Biol 134:269–284

  43. Largiadèr CR, Fries V, Bakker TCM (2001) Genetic analysis of sneaking and egg-thievery in a natural population of the three-spined stickleback (Gasterosteus aculeatus L.). Heredity 86:459–468

  44. Laube JC, Newland MJ, Hogan C, Brenninkmeijer CA, Fraser PJ, Martinerie P, Oram DE, Reeves CE, Röckmann T, Schwander J (2014) Newly detected ozone-depleting substances in the atmosphere. Nat Geosci 7:266–269

  45. Le Cren E (1951) The length-weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). J Anim Ecol 20:201–219

  46. Lu XY, Wu RSS (2005a) Ultraviolet damages sperm mitochondrial function and membrane integrity in the sea urchin Anthocidaris crassispina. Ecotoxicol Environ Safe 61:53–59

  47. Lu XY, Wu RSS (2005b) UV induces reactive oxygen species, damages sperm, and impairs fertilisation in the sea urchin Anthocidaris crassispina. Mar Biol 148:51–57

  48. Madronich S, McKenzie RL, Björn LO, Caldwell MM (1998) Changes in biologically active ultraviolet radiation reaching the Earth’s surface. J Photochem Photobiol B 46:5–19

  49. Madronich S, Shao M, Wilson S, Solomon K, Longstreth J, Tang X (2015) Changes in air quality and tropospheric composition due to depletion of stratospheric ozone and interactions with changing climate: implications for human and environmental health. Photochem Photobiol Sci 14:149–169

  50. McFadzen I, Baynes S, Hallam J, Beesley A, Lowe D (2000) Histopathology of the skin of UV-B irradiated sole (Solea solea) and turbot (Scophthalmus maximus) larvae. Mar Environ Res 50:273–277

  51. McGraw KJ, Hill G (2006) Mechanics of carotenoid-based coloration. Bird Color 1:177–242

  52. Mehlis M, Bakker TCM (2013) Male reproductive traits of full-sibs of different age classes in three-spined sticklebacks (Gasterosteus aculeatus). SpringerPlus 2:175

  53. Mehlis M, Bakker TCM (2014) The influence of ambient water temperature on sperm performance and fertilization success in three-spined sticklebacks (Gasterosteus aculeatus). Evol Ecol 28:655–667

  54. Mehlis M, Frommen JG, Rahn AK, Bakker TCM (2012) Inbreeding in three-spined sticklebacks (Gasterosteus aculeatus L.): effects on testis and sperm traits. Biol J Lin Soc 107:510–520

  55. Mehlis M, Hilke LK, Bakker TCM (2013) Attractive males have faster sperm in three-spined sticklebacks Gasterosteus aculeatus. Curr Zool 59:761–768

  56. Mehlis M, Rick IP, Bakker TCM (2015) Dynamic resource allocation between pre- and postcopulatory episodes of sexual selection determines competitive fertilization success. Proc R Soc B 282:20151279

  57. Milinski M, Bakker TCM (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–333

  58. Mitchell DL, Fernandez AA, Nairn RS, Garcia R, Paniker L, Trono D, Thames HD, Gimenez-Conti I (2010) Ultraviolet A does not induce melanomas in a Xiphophorus hybrid fish model. Proc Natl Acad Sci 107:9329–9334

  59. Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92

  60. Montzka SA et al (2018) An unexpected and persistent increase in global emissions of ozone-depleting CFC-11. Nature 557:413–417

  61. Ota K, Heg D, Hori M, Kohda M (2010) Sperm phenotypic plasticity in a cichlid: a territorial male’s counterstrategy to spawning takeover. Behav Ecol 21:1293–1300

  62. Parker G (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567

  63. Parker GA (1990) Sperm competition games: raffles and roles. Proc R Soc Lond B 242:120–126

  64. Pike TW, Blount JD, Bjerkeng B, Lindström J, Metcalfe NB (2007) Carotenoids, oxidative stress and female mating preference for longer lived males. Proc R Soc Lond B 274:1591–1596

  65. Pike TW, Bjerkeng B, Blount JD, Lindström J, Metcalfe NB (2011) How integument colour reflects its carotenoid content: a stickleback’s perspective. Funct Ecol 25:297–304

  66. Rahman MM, Turchini GM, Gasparini C, Norambuena F, Evans JP (2014) The expression of pre- and postcopulatory sexually selected traits reflects levels of dietary stress in guppies. PLoS One 9:e105856

  67. Ravishankara A, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125

  68. R Core Team (2017) R: a language and environment for statistical com-puting. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 27 Oct 2017

  69. Rick IP, Bakker TCM (2008) Males do not see only red: UV wavelengths and male territorial aggression in the three-spined stickleback (Gasterosteus aculeatus). Naturwissenschaften 95:631–638

  70. Rick IP, Modarressie R, Bakker TCM (2006) UV wavelengths affect female mate choice in three-spined sticklebacks. Anim Behav 71:307–313

  71. Rick IP, Mehlis M, Bakker TCM (2011) Male red ornamentation is associated with female red sensitivity in sticklebacks. PLoS One 6:e25554

  72. Rick IP, Mehlis M, Eßer E, Bakker TCM (2014) The influence of ambient ultraviolet light on sperm quality and sexual ornamentation in three-spined sticklebacks (Gasterosteus aculeatus). Oecologia 174:393–402

  73. Rowe MP, Baube CL, Loew ER, Phillips JB (2004) Optimal mechanisms for finding and selecting mates: how threespine stickleback (Gasterosteus aculeatus) should encode male throat colors. J Comp Physiol A 190:241–256

  74. Seaver RW, Ferguson GW, Gehrmann WH, Misamore MJ (2009) Effects of ultraviolet radiation on gametic function during fertilization in zebra mussels (Dreissena polymorpha). J Shellfish Res 28:625–633

  75. Sheldon B (1994) Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proc R Soc Lond B 257:25–30

  76. Singh K, Samant MA, Tom MT, Prasad NG (2016) Evolution of pre- and post-copulatory traits in male Drosophila melanogaster as a correlated response to selection for resistance to cold stress. PLoS One 11:e0153629

  77. Sokolowska E, Kulczykowska E (2006) Annual reproductive cycle in two free living populations of three-spined stickleback (Gasterosteus aculeatus L.): patterns of ovarian and testicular development. Oceanologia 48:103–124

  78. Solomon S (2004) The hole truth. Nature 427:289–291

  79. Stockley P, Gage MJG, Parker GA, Møller AP (1997) Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am Nat 149:933–954

  80. Stoddard MC, Prum RO (2008) Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of new world buntings. Am Nat 171:755–776

  81. Surmacki A (2008) Preen waxes do not protect carotenoid plumage from bleaching by sunlight. Ibis 150:335–341

  82. Tomášek O, Albrechtová J, Němcová M, Opatová P, Albrecht T (2017) Trade-off between carotenoid-based sexual ornamentation and sperm resistance to oxidative challenge. Proc R Soc B 284:20162444

  83. Vitt S, Rahn AK, Drolshagen L, Bakker TCM, Scharsack JP, Rick IP (2017a) Enhanced ambient UVB light affects growth, body condition and the investment in innate and adaptive immunity in three-spined sticklebacks (Gasterosteus aculeatus). Aquat Ecol 51:499–509

  84. Vitt S, Zierul JE, Bakker TCM, Rick IP (2017b) Long-term UVB exposure promotes predator-inspection behaviour in a fish. Biol Lett 13:20170497

  85. Weatherhead EC, Andersen SB (2006) The search for signs of recovery of the ozone layer. Nature 441:39–45

  86. Williamson CE, Zepp RG, Lucas RM, Madronich S, Austin AT, Ballaré CL, Norval M, Sulzberger B, Bais AF, McKenzie RL (2014) Solar ultraviolet radiation in a changing climate. Nat Clim Change 4:434–441

  87. Wootton RJ (1984) A functional biology of sticklebacks. Croom Helm, London

  88. Zagarese HE, Williamson CE (2001) The implications of solar UV radiation exposure for fish and fisheries. Fish Fish 2:250–260

  89. Zan-Bar T, Bartoov B, Segal R, Yehuda R, Lavi R, Lubart R, Avtalion R (2005) Influence of visible light and ultraviolet irradiation on motility and fertility of mammalian and fish sperm. Photomed Laser Surg 23:549–555

  90. Zbinden M, Largiadèr CR, Bakker TCM (2001) Sperm allocation in the three-spined stickleback. J Fish Biol 59:1287–1297

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We are grateful to the ‘Bakker’ research group for discussion and Jan Hottentot for catching sticklebacks in the field. We also thank Aaron Wirsing and three anonymous reviewers for their comments on earlier versions of this paper.

Author information

SV, TCMB and IPR designed the study. SV and MM-R collected the data. SV and IPR did the statistical analyses. SV wrote the manuscript supported by MM-R, TCMB and IPR.

Correspondence to Simon Vitt.

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Communicated by Aaron J Wirsing.

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Vitt, S., Mehlis-Rick, M., Bakker, T.C.M. et al. Enhanced ambient UVB radiation affects post-mating, but not pre-mating sexual traits in a fish. Oecologia 190, 355–366 (2019). https://doi.org/10.1007/s00442-019-04422-z

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  • Ultraviolet light
  • Breeding colouration
  • Sperm movement
  • Sperm morphology
  • Sexual selection