Advertisement

Marine Biology

, 166:37 | Cite as

Differential investment in male accessory glands: lessons from a marine fish with alternative reproductive tactics

  • Jessica S. MillerEmail author
  • Carlotta Mazzoldi
  • Maria B. Rasotto
  • Sigal Balshine
Original paper

Abstract

Male reproductive accessory glands play a number of important roles, including enhancing fertilization success in competitive contexts. Theory predicts that males experiencing greater sperm competition risk (i.e. those adopting the opportunistic tactic) should invest more in accessory glands and ejaculate. However, empirical data show the opposite pattern; males experiencing lower sperm competition risk (i.e. those adopting the conventional guarder tactic) invest more in accessory glands. This pattern has possibly emerged because these organs also function to optimize sperm economy and sometimes also play a role in parental care, which provides more benefits to guarder males. To tease apart these contrasting patterns, we examined tactic-specific investment in and histology of accessory glands, as well as the effect of their fluids on sperm performance in guarder males, using the plainfin midshipman fish (Porichthys notatus). We found that midshipman accessory glands consist of two distinct structures: nodes and lobules, differing in organization and secretory characteristics both between structures and male types. Like other fishes with alternative reproductive tactics, guarder males invested more in accessory glands and in lobules specifically compared to opportunistic sneaker males. Fluids from both lobule and nodes increased sperm velocity in guarder males. Moreover, guarder males increased their investment in accessory glands across the breeding season. Our results suggest that accessory glands may have multiple functions and may even play a role in parental care and olfactory signalling. Our study emphasizes the diversity in form and function of accessory glands and highlights the importance of these organs in reproduction.

Notes

Acknowledgements

We would like to thank Stz’uminius First Nations for their permission to sample at Ladysmith Inlet, and P. Walker and R. Shepherd for granting us access to our field site. We also thank the University of Victoria OAU and Animal Care staff, H. Hicklin and Dr. H. Kreiberg at the Pacific Biological Station in Nanaimo, BC, as well as Dr. F. Juanes, K. Cox, and Dr. J. S. Taylor for logistical support. We are extremely grateful to Drs. A. P. H. Bose, K. M. Cogliati, J. L. Fitzpatrick, and N. Sopinka for their comprehensive field work, as well as to N. Houpt, E. Sadler, T. Warriner, N. Luymes, E. Balke, H. Kou, H. Howe, A. Hassan, A. Mistakidis, Dr. J. Marentette, and Dr. J. Taves for their assistance in the field and with data collection. We thank C. Breggion for aid with histological analyses and Dr. J. L. Fitzpatrick and Dr. T. Pitcher for their many suggestions and guidance on sperm collection and analysis techniques. We would also like to thank Dr. B. Bolker, Dr. J. Dushoff, and the McMaster “data lunch” crew for their SAGE statistical suggestions, as well as S. Gotic for data processing help. We also thank our three anonymous reviewers for their helpful input and suggestions.

Funding

This research was supported by grants from the Natural Science and Engineering Research Council of Canada (Grant no. 10538042), the American Museum of Natural History, and from the Department of Psychology, Neuroscience, and Behaviour and the School of Graduate Studies at McMaster University.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interest.

Ethical standards

Plainfin midshipman fish are a common intertidal species and their populations are not endangered or threatened. All fish were collected in accordance with permits issued by the Canadian Department of Fisheries and Oceans (scientific licenses XR 50 2010, XR 126 2011, XR 14 2013, XR 121 2014, XR 81 2015, XR 94 2016, and XR 58 2017). All research procedures were approved by the McMaster University Animal Research Ethics Board (AUP’s #10-11-70 and #13-12-52) and the University of Victoria Animal Care Committee (Protocols 2015-009[1] and 2017-003[1]).

Supplementary material

227_2019_3474_MOESM1_ESM.docx (23 kb)
Supplementary material 1 (DOCX 23 kb)

References

  1. Adiyodi KG, Adiyodi RG (1988) Reproductive biology of invertebrates, accessory sex glands, vol III. Wiley, ChichesterGoogle Scholar
  2. Barni A, Mazzoldi C, Rasotto MB (2001) Reproductive apparatus and male accessory structures in two batrachoid species (Teleostei, Batrachoididae). J Fish Biol 58:1557–1569.  https://doi.org/10.1006/jfbi.2001.1560 CrossRefGoogle Scholar
  3. Bates D, Machler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  4. Birkhead TR, Moller AP (1998) Sperm competition and sexual selection. Academic Press, LondonGoogle Scholar
  5. Bose APH, McClelland GB, Balshine S (2015) Cannibalism, competition, and costly care in the plainfin midshipman fish, Porichthys notatus. Behav Ecol 27:628–636.  https://doi.org/10.1093/beheco/arv203 CrossRefGoogle Scholar
  6. Brantley RK, Bass AH (1994) Alternative male spawning tactics and acoustic signals in the plainfin midshipman fish Porichthys notatus Girard (Teleostei, Batrachoididae). Ethology 96:213–232.  https://doi.org/10.1111/j.1439-0310.1994.tb01011.x CrossRefGoogle Scholar
  7. Brantley RK, Tseng J, Bass AH (1993) The ontogeny of inter- and intrasexual vocal muscle dimorphisms in a sound-producing fish. Brain Behav Evol 42:336–349CrossRefGoogle Scholar
  8. Chapman T (2008) The soup in my fly: evolution, form and function of seminal fluid proteins. PLoS Biol 6:1379–1382.  https://doi.org/10.1371/journal.pbio.0060179 CrossRefGoogle Scholar
  9. Chowdhury I, Joy KP (2007) Seminal vesicle and its role in the reproduction of teleosts. Fish Physiol Biochem 33:383–398.  https://doi.org/10.1007/s10695-007-9162-5 CrossRefGoogle Scholar
  10. Ciereszko A, Dietrich MA, Nynca J (2017) Fish semen proteomics—new opportunities in fish reproductive research. Aquaculture 472:81–92.  https://doi.org/10.1016/j.aquaculture.2016.03.005 CrossRefGoogle Scholar
  11. Cogliati KM, Neff BD, Balshine S (2013) High degree of paternity loss in a species with alternative reproductive tactics. Behav Ecol Sociobiol 67:399–408.  https://doi.org/10.1007/s00265-012-1460-y CrossRefGoogle Scholar
  12. Cogliati KM, Balshine S, Neff BD (2014) Competition and cuckoldry: estimating fitness of alternative reproductive tactics in plainfin midshipman. Behaviour 151:1209–1227.  https://doi.org/10.1163/1568539X-00003180 CrossRefGoogle Scholar
  13. Colombo L, Marconato A, Belvedere PC, Friso C (1980) Endocrinology of teleost reproduction: a testicular steroid pheromone in the black goby, Gobius jozo L. Bolletino di Zool 47:355–364.  https://doi.org/10.1080/11250008009438692 CrossRefGoogle Scholar
  14. den Boer Susanne PA, Baer B, Boomsma Jacobus J (2010) Seminal fluid mediates ejaculate competition in social insects. Sci Rep 327:1506–1509.  https://doi.org/10.5061/dryad.5t110.supplementary CrossRefGoogle Scholar
  15. Fitzpatrick JL, Desjardins JK, Milligan N, Montgomerie R, Balshine S (2007) Reproductive-tactic-specific variation in sperm swimming speeds in a shell-brooding cichlid. Biol Reprod 77:280–284.  https://doi.org/10.1095/biolreprod.106.059550 CrossRefPubMedGoogle Scholar
  16. Fitzpatrick JL, Earn DJD, Bucking C, Craig PM, Nadella S, Wood CM, Balshine S (2015) Postcopulatory consequences of female mate choice in a fish with alternative reproductive tactics. Behav Ecol.  https://doi.org/10.1093/beheco/arv159 CrossRefGoogle Scholar
  17. Flannery EW, Butts IAE, Słowińska M, Ciereszko A, Pitcher TE (2013) Reproductive investment patterns, sperm characteristics, and seminal plasma physiology in alternative reproductive tactics of Chinook salmon (Oncorhynchus tshawytscha). Biol J Linn Soc 108:99–108.  https://doi.org/10.1111/j.1095-8312.2012.01980.x CrossRefGoogle Scholar
  18. Giacomello E, Marchini D, Rasotto MB (2006) A male sexually dimorphic trait provides antimicrobials to eggs in blenny fish. Biol Lett 2:330–333.  https://doi.org/10.1098/rsbl.2006.0492 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Giacomello E, Neat FC, Rasotto MB (2008a) Mechanisms enabling sperm economy in blenniid fishes. Behav Ecol Sociobiol 62:671–680.  https://doi.org/10.1007/s00265-007-0491-2 CrossRefGoogle Scholar
  20. Giacomello E, Marri L, Marchini D, Mazzoldi C, Rasotto MB (2008b) Sperm-duct gland secretion of the grass goby Zosterisessor ophiocephalus exhibits antimicrobial activity. J Fish Biol 73:1823–1828.  https://doi.org/10.1111/j.1095-8649.2008.02069.x CrossRefGoogle Scholar
  21. Gombar R, Pitcher TE, Lewis JA, Auld J, Vacratsis PO (2017) Proteomic characterization of seminal plasma from alternative reproductive tactics of Chinook salmon (Oncorhynchus tswatchysha). J Proteom 157:1–9.  https://doi.org/10.1016/j.jprot.2017.01.019 CrossRefGoogle Scholar
  22. Hong WS, Chen SX, Zhang QY, Zheng WY (2006) Sex organ extracts and artificial hormonal compounds as sex pheromones to attract broodfish and to induce spawning of Chinese black sleeper (Bostrichthys sinensis Lacepede). Aquac Res 37:529–534.  https://doi.org/10.1111/j.1365-2109.2006.01462.x CrossRefGoogle Scholar
  23. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363.  https://doi.org/10.1002/bimj.200810425 CrossRefGoogle Scholar
  24. Hyman LH (1992) Hyman’s comparative vertebrate anatomy, 3rd edn. The University of Chicago Press, ChicagoGoogle Scholar
  25. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw.  https://doi.org/10.18637/jss.v082.i13 CrossRefGoogle Scholar
  26. Lambert JGD, Resink JW (1991) Steroid glucuronides as male pheromones in the reproduction of the African catfish Clarias gariepinus—a brief review. J Steroid Biochem Mol Biol 40:549–556.  https://doi.org/10.1016/0960-0760(91)90276-B CrossRefPubMedGoogle Scholar
  27. Lewis JA, Pitcher TE (2017) The effects of rival seminal plasma on sperm velocity in the alternative reproductive tactics of Chinook salmon. Theriogenology 92:24–29.  https://doi.org/10.1016/j.theriogenology.2016.12.032 CrossRefPubMedGoogle Scholar
  28. Locatello L, Mazzoldi C, Rasotto MB (2002) Ejaculate of sneaker males is pheromonally inconspicuous in the black goby, Gobius niger (Teleostei, Gobiidae). J Exp Zool 293:601–605.  https://doi.org/10.1002/jez.10168 CrossRefPubMedGoogle Scholar
  29. Locatello L, Poli F, Rasotto MB (2013) Tactic-specific differences in seminal fluid influence sperm performance. Proc R Soc B 280:20122891.  https://doi.org/10.1098/rspb.2012.2891 CrossRefPubMedGoogle Scholar
  30. Marentette JR, Fitzpatrick JL, Berger RG, Balshine S (2009) Multiple male reproductive morphs in the invasive round goby (Apollonia melanostoma). J Great Lakes Res 35:302–308.  https://doi.org/10.1016/j.jglr.2009.01.009 CrossRefGoogle Scholar
  31. Mazzoldi C, Rasotto MB (2002) Alternative male mating tactics in Gobius niger. J Fish Biol 61:157–172.  https://doi.org/10.1111/j.1095-8649.2002.tb01743.x CrossRefGoogle Scholar
  32. Miller JS, Bose APH, Fitzpatrick JL, Balshine S (2019) Sperm maturation and male tactic-specific differences in ejaculates in a marine fish. J Fish Biol (in press) Google Scholar
  33. Modesto T, Canário AVM (2003) Morphometric changes and sex steroid levels during the annual reproductive cycle of the Lusitanian toadfish, Halobatrachus didactylus. Gen Comp Endocrinol 131:220–231.  https://doi.org/10.1016/S0016-6480(03)00027-3 CrossRefPubMedGoogle Scholar
  34. Modesto T, Freitas AMMS, Canário AVM (2015) Steroidogenesis by testis and accessory glands of the Lusitanian toadfish, Halobatrachus didactylus, during reproductive season. Gen Comp Endocrinol 223:120–128.  https://doi.org/10.1016/j.ygcen.2015.09.026 CrossRefPubMedGoogle Scholar
  35. Neat FC (2001) Male parasitic spawning in two species of triplefin blenny (Tripterigiidae): contrasts in demography, behaviour and gonadal characteristics. Environ Biol Fishes 61:57–64.  https://doi.org/10.1023/A:1011074716758 CrossRefGoogle Scholar
  36. Neat FC, Locatello L, Rasotto MB (2003) Reproductive morphology in relation to alternative male reproductive tactics in Scartella cristata. J Fish Biol 62:1381–1391.  https://doi.org/10.1046/j.1095-8649.2003.00122.x CrossRefGoogle Scholar
  37. Neff BD, Fu P, Gross MR (2003) Sperm investment and alternative mating tactics in bluegill sunfish (Lepomis macrochirus). Behav Ecol 14:634–641.  https://doi.org/10.1093/beheco/arg032 CrossRefGoogle Scholar
  38. Oliveira RF, Canario AV, Grober MS (2001) Male sexual polymorphism, alternative reproductive tactics, and androgens in combtooth blennies (Pisces: Blenniidae). Horm Behav 40:266–275.  https://doi.org/10.1006/hbeh.2001.1683 CrossRefPubMedGoogle Scholar
  39. Olsson M, Schwartz T, Uller T, Healey M (2009) Effects of sperm storage and male colour on probability of paternity in a polychromatic lizard. Anim Behav 77:419–424.  https://doi.org/10.1016/j.anbehav.2008.10.017 CrossRefGoogle Scholar
  40. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol J Linn Soc 45:525–567.  https://doi.org/10.1111/j.1469-185X.1970.tb01176.x CrossRefGoogle Scholar
  41. Parker GA (1990) Sperm competition games: sneaks and extra-pair copulations. Proc R Soc B 242:127–133.  https://doi.org/10.1098/rspb.1990.0115 CrossRefGoogle Scholar
  42. Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, London, pp 3–49CrossRefGoogle Scholar
  43. Parker GA, Pizzari T (2010) Sperm competition and ejaculate economics. Biol Rev 85:897–934.  https://doi.org/10.1111/j.1469-185X.2010.00140.x CrossRefPubMedGoogle Scholar
  44. Pearse AG (1950) Histochemistry. Theoretical and applied analytical technology, 4th edn. Churchill Livingstone, LondonGoogle Scholar
  45. Pitnick S, Hosken DJ, Birkhead TR (2009) Sperm morphological diversity. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic Press, Oxford, pp 69–149CrossRefGoogle Scholar
  46. Pizzolon M, Giacomello E, Marri L, Marchini D, Pascoli F, Mazzoldi C, Rasotto MB (2010) When fathers make the difference: efficacy of male sexually selected antimicrobial glands in enhancing fish hatching success. Funct Ecol 24:141–148.  https://doi.org/10.1111/j.1365-2435.2009.01608.x CrossRefGoogle Scholar
  47. Poiani A (2006) Complexity of seminal fluid: a review. Behav Ecol Sociobiol 60:289–310.  https://doi.org/10.1007/s00265-006-0178-0 CrossRefGoogle Scholar
  48. Poli F, Locatello L, Rasotto MB (2018) Seminal fluid enhances competitiveness of territorial males’ sperm in a fish with alternative male reproductive tactics. J Exp Biol.  https://doi.org/10.1242/jeb.175976 CrossRefPubMedGoogle Scholar
  49. Ramm SA, Parker GA, Stockley P (2005) Sperm competition and the evolution of male reproductive anatomy in rodents. Proc R Soc B Biol Sci 272:949–955.  https://doi.org/10.1098/rspb.2004.3048 CrossRefGoogle Scholar
  50. Rasotto MB (unpublished) Form and function in the male reproductive apparatus of teleost fishesGoogle Scholar
  51. Rasotto MB, Mazzoldi C (2002) Male traits associated with alternative reproductive tactics in Gobius niger. J Fish Biol 61:173–184.  https://doi.org/10.1111/j.1095-8649.2002.tb01744.x CrossRefGoogle Scholar
  52. Scaggiante M, Mazzoldi C, Petersen CW, Rasotto MB (1999) Sperm competition and mode of fertilization in the grass goby Zosterisessor ophiocephalus (Teleostei: Gobiidae). J Exp Zool 283:81–90.  https://doi.org/10.1002/(SICI)1097-010X(19990101)283:1%3c81:AID-JEZ9%3e3.0.CO;2-9 CrossRefGoogle Scholar
  53. Serrano RM, Lopes O, Hubbard PC, Araujo J, Canario AVM, Barata EN (2008a) 11-Ketotestosterone stimulates putative sex pheromone production in the male peacock blenny, Salaria pavo (Risso 1810). Biol Reprod 79:861–868.  https://doi.org/10.1095/biolreprod.108.069914 CrossRefPubMedGoogle Scholar
  54. Serrano RM, Barata EN, Birkett MA, Hubbard PC, Guerreiro PA, Canario AVM (2008b) Behavioral and olfactory responses of female Salaria pavo (Pisces: Blenniidae) to a putative multi-component male pheromone. J Chem Ecol 34:647–658.  https://doi.org/10.1007/s10886-008-9466-7 CrossRefPubMedGoogle Scholar
  55. Setchell JM (2008) Alternative reproductive tactics in primates. In: Oliveria RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics: an integrative approach. Cambridge University Press, Cambridge, pp 373–398CrossRefGoogle Scholar
  56. Simmons LW, Fitzpatrick JL (2012) Sperm wars and the evolution of male fertility. Reproduction 144:519–534.  https://doi.org/10.1530/REP-12-0285 CrossRefPubMedGoogle Scholar
  57. Simmons LW, Emlen DJ, Tomkins JL (2007) Sperm competition games between sneaks and guards: a comparative analysis using dimorphic male beetles. Evolution (New York) 61:2684–2692.  https://doi.org/10.1111/j.1558-5646.2007.00243.x CrossRefGoogle Scholar
  58. Smith RL (2012) Sperm competition and the evolution of animal mating systems. Academic Press, LondonGoogle Scholar
  59. Taborsky M (1994) Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Adv Study Behav 23:1–100.  https://doi.org/10.1016/S0065-3454(08)60351-4 CrossRefGoogle Scholar
  60. Taborsky M (1998) Sperm competition in fish: ‘bourgeois’ males and parasitic spawning. Trends Ecol Evol 13:222–227.  https://doi.org/10.1016/S0169-5347(97)01318-9 CrossRefPubMedGoogle Scholar
  61. Taborsky M (2008) Alternative reproductive tactics in fish. In: Oliveria RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics: an integrative approach. Cambridge University Press, Cambridge, pp 251–299CrossRefGoogle Scholar
  62. Taborsky M, Oliveira RF, Brockmann HJ (2008) The evolution of alternative reproductive tactics: concepts and questions. In: Oliveria RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics: an integrative approach. Cambridge University Press, Cambridge, pp 1–21Google Scholar
  63. Utne-Palm AC, Eduard K, Jensen KH, Mayer I, Jakobsen PJ (2015) Size dependent male reproductive tactic in the two-spotted goby (Gobiusculus flavescens). PLoS One 1:1.  https://doi.org/10.1371/journal.pone.0143487 CrossRefGoogle Scholar
  64. Wigby S, Sirot LK, Linklater JR, Buehner N, Calboli FCF, Bretman A, Wolfner MF, Chapman T (2009) Seminal fluid protein allocation and male reproductive success. Curr Biol 19:751–757.  https://doi.org/10.1016/j.cub.2009.03.036 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Psychology, Neuroscience, & BehaviourMcMaster UniversityHamiltonCanada
  2. 2.Department of BiologyUniversity of PadovaPaduaItaly

Personalised recommendations