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Determination of the Female-Biased Sex Ratio in Some Young-of-the-Year and Spawner Samples of the Threespine Stickleback Gasterosteus aculeatus by Environmental, Not Genetic, Factors

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Abstract

Genetic markers (sex-specific loci of Ga1 and Ga2) have been used to analyze the sex ratio of the threespine stickleback at different stages of ontogenesis. The progeny of all individually tested females includes both males and females, and no significant departures from a 1 : 1 sex ratio has been found in embryos from the natural nests. Juveniles did not demonstrate a sex bias up to one-and-a-half or two months of age, but in older juveniles, females prevailed (this fact has been reported for the first time). Females prevail among spawners, which mostly results from the predominant elimination of males during the spawning and post-spawning periods. The possible causes of this predominance are discussed.

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REFERENCES

  1. Aneer, G., Biometrical characteristics of the three-spined stickleback (Gasterosteus aculeatus L.) from Northern Baltic proper, Zool. Scr., 1973, vol. 2, pp. 157–162.

    Google Scholar 

  2. Arnold, K.E., Adam, A., Orr, K.J., Griffiths, R., and Barber, I., Sex-specific survival and parasitism in three-spined sticklebacks: seasonal patterns revealed by molecular analysis, J. Fish Biol., 2003, vol. 63, pp. 1046–1050.

    Google Scholar 

  3. Bakhvalova, A.E., Ivanova, T.S., Ivanov, M.V., Demchuk, A.S., Movchan, E.A., and Lajus, D.L., Long-term changes in the role of threespine stickleback (Gasterosteus aculeatus) in the White Sea: predatory fish consumption reflects fluctuating stickleback abundance during the last century, Evol. Ecol. Res., 2016, vol. 17, pp. 317–334.

    Google Scholar 

  4. Bakker, T.C.M., No evidence of sex reversal by means of experimentally altered sex ratios in threespine stickleback, Evol. Ecol. Res., 2016, vol. 17, pp. 291–300.

    Google Scholar 

  5. Bakker, T.C.M., Giger, T., Frommen, J.G., and Largiadèr, C.R., Rapid molecular sexing of three-spined sticklebacks, Gasterosteus aculeatus L., based on large Y-chromosomal insertions, J. Appl. Genet., 2017, vol. 58, pp. 401–407.

    CAS  PubMed  Google Scholar 

  6. Bell, M.A. and Aguirre, W.E., Contemporary evolution, allelic recycling, and adaptive radiation of the threespine stickleback, Evol. Ecol. Res., 2013, vol. 15, pp. 377–411.

    Google Scholar 

  7. Bell, A.M., Dingermanse, N.J., Hankison, S.J., Langenhof, M.B.W., and Rollins, K., Early exposure to nonlethal predation risk by size-selective predators increases somatic growth and decreases size at adulthood in threespined sticklebacks, J. Evol. Biol., 2011, vol. 24, pp. 943–953.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Bernhardt, R.R., von Hippel, F.A., and Cresko, W.A., Perchlorate induces hermaphroditism in threespine sticklebacks, Environ. Toxicol. Chem., 2006, vol. 25, pp. 2087–2096.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Bissegger, M., Laurentino, T.G., Roesti, M., and Berner, D., Widespread intersex differentiation across the stickleback genome—the signature of sexually antagonistic selection?, Mol. Ecol., 2020, vol. 29, pp. 262–271.

    CAS  PubMed  Google Scholar 

  10. Brykov, V.A., Mechanisms of sex determination in fish: evolutionary and practical aspects, Russ. J. Mar. Ecol., 2014, vol. 40, no. 6, pp. 407–417.

    Google Scholar 

  11. Dean, L.L., Robertson, S., Mahmud, M., and MacColl, A.D.C., Internal embryonic development in a non-copulatory, egg-laying teleost, the three-spined stickleback, Gasterosteus aculeatus, Sci. Rep., 2019, vol. 9, p. 2395.

    PubMed  PubMed Central  Google Scholar 

  12. Demchuk, A.S., Ivanov, M.V., Ivanova, T.S., Polyakova, N.V., Golovin, P.V., and Lajus, D.L., Feeding of the White Sea three-spined stickleback Gasterosteus aculeatus (Linnaeus, 1758) in spawning grounds, Tr. Karel. Nauchn. Tsentra Ross. Akad. Nauk. 2018, no. 4, pp. 42–58.

  13. Devlin, R.H. and Nagahama, Y., Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences, Aquaculture, 2002, vol. 208, pp. 191–364.

    CAS  Google Scholar 

  14. Furin, C.G., von Hippel, F.A., Postlethwait, J.H., Buck, C.L., Cresko, W.A., and O’Hara, T.M., Developmental timing of sodium perchlorate exposure alters angiogenesis, thyroid follicle proliferation and sexual maturation in stickleback, Gen. Comp. Endocrinol., 2015, vol. 219, pp. 24–35.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Geodakyan, V.A Sex chromosomes: what are they for? (New concept), Dokl. Akad. Nauk, 1996, vol. 346, no. 4, pp. 565–569.

    CAS  Google Scholar 

  16. Gibson, G., The synthesis and evolution of a supermodel, Science, 2005, vol. 307, pp. 1890–1891.

    CAS  PubMed  Google Scholar 

  17. Golovin, P.V., Bakhvalova, A.E., Ivanov, M.V., Ivanova, T.S., Smirnova, K.A., and Lajus, D.L., Sex-biased mortality of marine threespine stickleback (Gasterosteus aculeatus L.) during their spawning period in the White Sea, Evol. Ecol. Res., 2019, vol. 20, pp. 279–295.

    Google Scholar 

  18. Griffiths, R., Orr, K.J., Adam, A., and Barber, I., DNA sex identification in the three-spined stickleback, J. Fish Biol., 2000, vol. 57, pp. 1331–1334.

    CAS  Google Scholar 

  19. Hagen, D.W. and Gilbertson, L.G., Selective predation and intensity of selection acting upon the lateral plates of threespine stickleback, Heredity, 1973, vol. 30, pp. 273–287.

    Google Scholar 

  20. Hahlbeck, E., Griffiths, R., and Bengtsson, B.-E., The juvenile three-spined stickleback (Gasterosteus aculeatus L.) as a model organism for endocrine disruption. I. Sexual differentiation, Aquat. Toxicol., 2004, vol. 70, pp. 287–310.

    CAS  PubMed  Google Scholar 

  21. Hendry, A.P., Peichel, C.L., Matthews, B., Boughman, J.W., and Nosil, P., Stickleback research: the now and the next, Evol. Ecol. Res., 2013, vol. 15, pp. 111–141.

    Google Scholar 

  22. Heule, C., Salzburger, W., and Böhne, A., Genetics of sexual development: an evolutionary playground for fish, Genetics, 2014, vol. 196, pp. 579–591

    PubMed  PubMed Central  Google Scholar 

  23. Huntingford, F.A., Wright, P.J., and Tierney, J.F., Adaptive variation in antipredator behavior in threespined stickleback, in The Evolutionary Biology of Threespine Stickleback, Bell, M.A. and Foster, S.A., Eds., Oxford: Oxford Univ. Press, 1994, pp. 277–296.

    Google Scholar 

  24. Ivanova, T.S., Ivanov, M.V., Golovin, P.V., Polyakova, N.V., and Lajus, D.L., The White Sea threespine stickleback population: spawning habitats, mortality, and abundance, Evol. Ecol. Res., 2016, vol. 17, pp. 301–315.

    Google Scholar 

  25. Johnson, S. and Candolin, U., Predation cost of a sexual signal in the threespine stickleback, Behav. Ecol., 2017, vol. 28, pp. 1160–1165.

    Google Scholar 

  26. King, A.J., Fürtbauer, I., Mamuneas, D., James, C., and Manica, A., Sex-differences and temporal consistency in stickleback fish boldness, PLoS One, 2013, vol. 8, p. 81116. https://doi.org/10.1371/journal.pone.0081116

    Article  CAS  Google Scholar 

  27. Kynard, B.E., Breeding behavior of a lacustrine population of threespine sticklebacks (Gasterosteus aculeatus L.), Behaviour, 1978, vol. 67, pp. 178–207.

    Google Scholar 

  28. Lajus, D., Ivanova, T., Rybkina, E., Lajus, J., and Ivanov, M., Multidecadal fluctuations of threespine stickleback in the White Sea and their correlation with temperature, ICES J. Mar. Sci., 2021, vol. 78, pp. 653–665. https://doi.org/10.1093/icesjms/fsaa192

    Google Scholar 

  29. Lajus, D.L., Golovin, P.V., Zelenskaya, A.E., Demchuk, A.S., Dorgam, A.S., Ivanov, M.V., Ivanova, T.S., Murzina, S.A., Polyakova, N.V., Rybkina, E.V., and Yurtseva, A.O., Threespine stickleback of the White Sea: population characteristics and role in the ecosystem, Contemp. Probl. Ecol., 2020, vol. 13, no. 2, pp. 132–145.

    Google Scholar 

  30. Lindsey, C.C., Experimental study of meristic variation in a population of threespined stickleback, Gasterosteus aculeatus, Can. J. Zool., 1962, vol. 40, pp. 271–312.

    Google Scholar 

  31. Mukhomediyarov, F.B., Three-spined stickleback (Gasterosteus aculeatus L.) of the Kandalaksha Bay of the White Sea, Vopr. Ikhtiol., 1966, vol. 36, no. 3, pp. 454–467.

    Google Scholar 

  32. Niksirat, H., Hatef, A., and Abdoli, A., Life cycle and feeding habits of the threespined stickleback Gasterosteus aculeatus (Linnaeus, 1758): an alien species in the southeast Caspian Sea, Int. Aquat. Res., 2010, vol. 2, pp. 97–104.

    Google Scholar 

  33. Östlund-Nilsson, S., Mayer, I., and Huntingford, F.A., Biology of the Three-Spine Stickleback, Boca Raton: CRC Press, 2007.

    Google Scholar 

  34. Paepke, H.-J., Die Stichlinge: Gasterosteidae, Magdeburg: Westarp-Wiss, 1996.

    Google Scholar 

  35. Patimar, R., Najafabadi, M.H., and Souraki, M.G., Life history features of the nonindigenous three-spined stickleback (Gasterosteus aculeatus Linnaeus, 1758) in the Gomishan wetland (southeast Caspian Sea, Iran), Turk. J. Zool., 2010, vol. 34, pp. 461–470.

    Google Scholar 

  36. Peichel, C.L., Ross, J.A., Matson, C.K., Dickson, M., Grimwood, J., Schmutz, J., Myers, R.M., Mori, S., Schluter, D., Kingsley, D.M., The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome, Curr. Biol., 2004, vol. 14, pp. 1416–1424.

    CAS  PubMed  Google Scholar 

  37. Pichugin, M.Yu., Sidorov, L.V., and Gritsenko, O.F., Specific biological and morphological features of the three-spined stickleback Gasterosteus aculeatus in waters of the Kuril Islands, J. Ichthyol., 2003, vol. 43, no. 2, pp. 221–229.

    Google Scholar 

  38. Ramler, D., Mitteroecker, P., Shama, L.N.S., Wegner, K.M., and Ahnelt, H., Nonlinear effects of temperature on body form and developmental canalization in the threespine stickleback, J. Evol. Biol., 2014, vol. 27, pp. 497–507.

    CAS  PubMed  Google Scholar 

  39. Reimchen, T.E. and Nosil, P., Ecological causes of sex-biased parasitism in threespine stickleback, Biol. J. Linn. Soc., 2001, vol. 73, pp. 51–63.

    Google Scholar 

  40. Rollins, J.L., Chiang, P., Waite, J.N., von Hippel, F.A., and Bell, M.A., Jacks and Jills: alternative life-history phenotypes and skewed sex ratio in anadromous threespine stickleback (Gasterosteus aculeatus), Evol. Ecol. Res., 2017, vol. 18, pp. 363–382.

    Google Scholar 

  41. Rybkina, E.V., Demchuk, A.S., Lajus, D.L., Ivanova, T.S., Ivanov, M.V., and Galaktionov, K.V., Dynamics of parasite community during early ontogenesis of marine threespine stickleback, Gasterosteus aculeatus, Evol. Ecol. Res., 2016, vol. 17, pp. 335–354.

    Google Scholar 

  42. Saat, T. and Turovski, A., Three-spined stickleback, Gasterosteus aculeatus L., in Fishes of Estonia, Ojaveer, E., Pihu, E., and Saat, T., Eds., Tallinn: Estonian Academy Publishers, 2003, pp. 274–280.

    Google Scholar 

  43. Samonte-Padilla, I.E., Eizaquirre, C., Scharsack, J.P., Lenz, T.L., and Milinski, M., Induction of diploid gynogenesis in an evolutionary model organism, the three-spined stickleback (Gasterosteus aculeatus), BMC Dev. Biol., 2011, pp. 11–55.

  44. Shul’man, S.S. and Shul’man-Al’bova, R.E., Parazity ryb Belogo morya (Parasites of Fishes of the White Sea), Moscow: Akad. Nauk SSSR, 1953.

  45. Toli, E.-A., Calboli, F., Shikano, T., and Merilä, J., A universal and reliable assay for molecular sex identification of three-spined sticklebacks (Gasterosteus aculeatus), Mol. Ecol. Res., 2016, vol. 16, pp. 1389–1400.

    CAS  Google Scholar 

  46. Velando, A., Costa, M.M., and Kim, S.-Y., Sex-specific phenotypes and metabolism-related gene expression in juvenile sticklebacks, Behav. Ecol., 2017, vol. 28, pp. 1553–1563.

    Google Scholar 

  47. Whoriskey, F.G. and FitzGerald, G.L., The effects of bird predation on an estuarine stickleback (Pisces: Gasterosteidae) community, Can. J. Zool., 1985, vol. 63, pp. 301–307.

    Google Scholar 

  48. Wootton, R.J. and Smith, C., Reproductive Biology of Teleost Fishes, Chichester: Wiley, 2015.

    Google Scholar 

  49. Wootton, R.J., Fletcher, D.A., Smith, C., and Whoriskey, F.G., A review of reproductive rates in sticklebacks in relation to parental expenditure and operational sex ratios, Behaviour, 1995, vol. 132, pp. 915–933.

    Google Scholar 

  50. Yershov, P. and Sukhotin, A., Age and growth of marine three-spined stickleback in the White sea 50 years after a population collapse, Polar Biol., 2015, vol. 38, pp. 1813–1823.

    Google Scholar 

  51. Yoshida, K., Makino, T., Yamaguchi, K., Shigenobu, S., Hasebe, M., Kawata, M., Kume, M., Mori, S., Peichel, C.L., Toyoda, A., Fujiyama, A., and Kitano, J., Sex chromosome turnover contributes to genomic divergence between incipient stickleback species, PLoS Genet., 2014, vol. 10. e1004223.

    PubMed  PubMed Central  Google Scholar 

  52. Yurtseva, A., Noreikiene, K., Lajus, D., Li, Z., Alapassi, T., Ivanova, T., Ivanov, M., Golovin, P., Vesala, S., and Merilä, J., Aging three-spined sticklebacks Gasterosteus aculeatus: comparison of estimates from three structures, J. Fish Biol., 2019, vol. 95, pp. 802–811.

    PubMed  Google Scholar 

  53. Zyuganov, V.V., Semeistvo kolyushkovykh (Gasterosteidae) mirovoi fauny (Family Gasterosteidae of the World Fauna), Leningrad: Nauka, 1991.

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This work was carried out with financial support from the Russian Science Foundation (project no. 19-14-00092).

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Correspondence to A. A. Makhrov.

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Translated by T. Kuznetsova

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Artamonova, V.S., Bardukov, N.V., Golovin, P.V. et al. Determination of the Female-Biased Sex Ratio in Some Young-of-the-Year and Spawner Samples of the Threespine Stickleback Gasterosteus aculeatus by Environmental, Not Genetic, Factors. Biol Bull Russ Acad Sci 48, 577–587 (2021). https://doi.org/10.1134/S1062359021050034

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