Advertisement

The overlapping reproductive traits of the two male mating types of the oval squid Sepioteuthis lessoniana

  • Chun-Yen Lin
  • Chih-Shin Chen
  • Chuan-Chin ChiaoEmail author
Original Article Biology

Abstract

The oval squid Sepioteuthis lessoniana is polyandrous, and a female mates with several males during a spawning season. This has resulted in two alternative male mating tactics in this species. The larger consort males usually use the male-parallel (MP) mating posture to put spermatophores at the opening of the oviduct; the smaller sneaker males predominantly use the male-upturned (MU) mating posture to place spermatophores around the female’s buccal membrane. Since squid eggs are released from the oviduct, MP mating is expected to have a higher fertilization rate than MU mating. Given the fact that these two male mating tactics are largely dependent on the body size of the male relative to the female, it is unclear how the smaller males are able to reproductively compete with the larger males. On analyzing spermatophore and sperm morphology from populations of adult male squids, spermatophore size was found to be positively correlated with mantle length of these squids, but sperm length was negatively correlated with squid mantle length. More importantly, no distinct size dimorphism exists in relation to either spermatophore morphology or sperm morphology. The overlap in size distributions of the spermatophores and sperms of the male squid thus implies that medium-sized males may have flexible reproductive strategies, switching between MP and MU mating tactics depending on the context of the mating event and/or female choice. This presumed behavioral plasticity might increase the reproductive success of these males and maintain the dynamic stability of two alternative mating types in this polyandrous species.

Keywords

Polyandry Sperm competition Alternative mating tactics Consort males Sneaker males 

Notes

Acknowledgements

We thank the fishermen of Ho-ping Island for their assistance with the collection of squid specimens. We also thank Ms. Jing-Yu Chen and Chiao-Wen Lin at the National Taiwan Ocean University for assistance in sample preparation and data processing. We are grateful for the invaluable comments from two anonymous reviewers. This study was supported by the Ministry of Science and Technology of Taiwan NSC-101-2313-B-019-001 (to CSC), and MOST 106-2311-B-007-010-MY3 (to CCC).

Supplementary material

12562_2018_1283_MOESM1_ESM.jpg (66 kb)
Figure S1. The age and mantle length in both cohorts are not correlated. (a) The selected samples from the 2012 Fall cohort. The correlation between age and mantle length was low. (b) The selected samples from 2013 Spring cohort. Similarly, the correlation between age and mantle length was low. Squid age was determined based on the statolith microstructure analysis (jpeg 65 kb)
12562_2018_1283_MOESM2_ESM.jpg (58 kb)
Figure S2. The fresh and fixed spermatophores and sperms are highly correlated. (a) The length of spermatophores was decreased slightly after fixation, but the correlation between fresh and fixed samples was high. (b) Similarly, the length of sperms was decreased slightly after fixation and sonication, but the correlation between fresh and fixed samples was high (jpeg 57 kb)

References

  1. Andersson MB (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  2. Birkhead TR, Martinez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc Lond B 266:1759–1764CrossRefGoogle Scholar
  3. Birkhead TR, Hosken DJ, Pitnick SS (2008) Sperm biology: an evolutionary perspective. Academic Press, LondonGoogle Scholar
  4. Boal JG (1997) Female choice of males in cuttlefish (Mollusca: Cephalopoda). Behaviour 134:975–988CrossRefGoogle Scholar
  5. Boyle PR, Ngoile MAK (1993) Assessment of maturity state and seasonality of reproduction in Loligo forbesi (Cephalopoda: Loliginidae) from Scottish waters. In: O’Dor R, Kubodera T, Okutani T (eds) Recent advances in cephalopod fisheries biology. Tokai University Press, Tokyo, pp 37–48Google Scholar
  6. Chen CS, Chen JY, Lin CW (2015) Variation in life-history traits for micro-cohorts of Sepioteuthis lessoniana in the waters off northern Taiwan. Fish Sci 81:53–64CrossRefGoogle Scholar
  7. Eberhard WG (1982) Beetle horn dimorphism: making the best of a bad lot. Am Nat 119:420–426CrossRefGoogle Scholar
  8. Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N, Balshine S (2009) Female promiscuity promotes the evolution of faster sperm in cichlid fishes. Proc Natl Acad Sci USA 106:1128–1132CrossRefGoogle Scholar
  9. Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA (2004) Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr Biol 14:44–47PubMedGoogle Scholar
  10. Gomendio M, Roldan ERS (2008) Implications of diversity in sperm size and function for sperm competition and fertility. Int J Dev Biol 52:439–447CrossRefGoogle Scholar
  11. Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92–98CrossRefGoogle Scholar
  12. Hall KC, Hanlon RT (2002) Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda). Mar Biol 140:533–545CrossRefGoogle Scholar
  13. Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, CambridgeGoogle Scholar
  14. Hanlon RT, Maxwell MR, Shashar N (1997) Behavioral dynamics that would lead to multiple paternity within egg capsules of the squid Loligo pealei. Biol Bull 193:212–214CrossRefGoogle Scholar
  15. Hanlon RT, Smale MJ, Sauer WHH (2002) The mating system of the squid Loligo vulgaris reynaudii (Cephalopoda, Mollusca) off South Africa: fighting, guarding, sneaking, mating and egg laying behavior. Bull Mar Sci 71:331–345Google Scholar
  16. Hanlon RT, Naud MJ, Shaw PW, Havenhand JN (2005) Behavioural ecology: transient sexual mimicry leads to fertilization. Nature 433:212CrossRefGoogle Scholar
  17. Hirohashi N, Iwata Y (2013) The different types of sperm morphology and behavior within a single species: why do sperm of squid sneaker males form a cluster? Commun Integr Biol 6:e26729CrossRefGoogle Scholar
  18. Hirohashi N, Alvarez L, Shiba K, Fujiwara E, Iwata Y, Mohri T, Inaba K, Chiba K, Ochi H, Supuran CT, Kotzur N, Kakiuchi Y, Kaupp UB, Baba SA (2013) Sperm from sneaker male squids exhibit chemotactic swarming to CO2. Curr Biol 23:775–781CrossRefGoogle Scholar
  19. Hirohashi N, Iwata Y, Sauer WH, Kakiuchi Y (2014) Respiratory CO2 mediates sperm chemotaxis in squids. In: Sawada H, Inoue N, Iwano M (eds) Sexual reproduction in animals and plants. Springer, New York, pp 13–21CrossRefGoogle Scholar
  20. Hirohashi N, Tamura-Nakano M, Nakaya F, Iida T, Iwata Y (2016) Sneaker male squid produce long-lived spermatozoa by modulating their energy metabolism. J Biol Chem 291:19324–19334CrossRefGoogle Scholar
  21. Huffard CL, Caldwell RL, Boneka F (2008) Mating behavior of Abdopus aculeatus (d’Orbigny 1834) (Cephalopoda: Octopodidae) in the wild. Mar Biol 154:353–362CrossRefGoogle Scholar
  22. Huffard CL, Caldwell RL, Boneka F (2010) Male–male and male–female aggression may influence mating associations in wild octopuses (Abdopus aculeatus). J Comp Psychol 124:38CrossRefGoogle Scholar
  23. Immler S, Pryke SR, Birkhead TR, Griffith SC (2010) Pronounced within-individual plasticity in sperm morphometry across social environments. Evolution 64:1634–1643CrossRefGoogle Scholar
  24. Iwata Y, Sakurai Y (2007) Threshold dimorphism in ejaculate characteristics in the squid Loligo bleekeri. Mar Ecol Prog Ser 345:141–146CrossRefGoogle Scholar
  25. Iwata Y, Munehara H, Sakurai Y (2005) Dependence of paternity rates on alternative reproductive behaviors in the squid Loligo bleekeri. Mar Ecol Prog Ser 298:219–228CrossRefGoogle Scholar
  26. Iwata Y, Shaw P, Fujiwara E, Shiba K, Kakiuchi Y, Hirohashi N (2011) Why small males have big sperm: dimorphic squid sperm linked to alternative mating behaviours. BMC Evol Biol 11:236CrossRefGoogle Scholar
  27. Iwata Y, Sakurai Y, Shaw P (2015) Dimorphic sperm-transfer strategies and alternative mating tactics in loliginid squid. J Molluscan Stud 81:147–151CrossRefGoogle Scholar
  28. Jantzen TM, Havenhand JN (2003) Reproductive behavior in the squid Sepioteuthis australis from South Australia: interactions on the spawning grounds. Biol Bull 204:305–317CrossRefGoogle Scholar
  29. Lin CY, Chiao CC (2017) Female choice leads to a switch in oval squid male mating tactics. Biol Bull 233:219–226CrossRefGoogle Scholar
  30. Mather J (2016) Mating games squid play: reproductive behaviour and sexual skin displays in Caribbean reef squid Sepioteuthis sepioidea. Mar Freshwat Behav Physiol 49:359–373CrossRefGoogle Scholar
  31. Moynihan M, Rodaniche AF (1982) The behavior and natural history of the caribbean reef squid Sepioteuthis sepioidea with a consideration of social, signal, and defensive patterns for difficult and dangerous environments. Paul Parey, BerlinGoogle Scholar
  32. Naud MJ, Hanlon RT, Hall KC, Shaw PW, Havenhand JN (2004) Behavioural and genetic assessment of reproductive success in a spawning aggregation of the Australian giant cuttlefish, Sepia apama. Anim Behav 67:1043–1050CrossRefGoogle Scholar
  33. Naud MJ, Sauer WH, McKeown NJ, Shaw PW (2016) Multiple mating, paternity and complex fertilisation patterns in the chokka squid Loligo reynaudii. PLoS ONE 11:e0146995CrossRefGoogle Scholar
  34. Neff BD, Svensson EI (2013) Polyandry and alternative mating tactics. Philos T R Soc B 368:20120045CrossRefGoogle Scholar
  35. Oliveira RF, Taborsky M, Brockmann HJ (2008) Alternative reproductive tactics: an integrative approach. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  36. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567CrossRefGoogle Scholar
  37. Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu Rev Ecol Evol Syst 36:125–146CrossRefGoogle Scholar
  38. Simmons LW, Tomkins JL, Hunt J (1999) Sperm competition games played by dimorphic male beetles. Proc R Soc Lond B 266:145–150CrossRefGoogle Scholar
  39. Taborsky M (1998) Sperm competition in fish: ‘bourgeois’ males and parasitic spawning. Trends Ecol Evol 13:222–227CrossRefGoogle Scholar
  40. Wada T, Takegaki T, Mori T, Natsukari Y (2005) Alternative male mating behaviors dependent on relative body size in captive oval squid Sepioteuthis lessoniana (Cephalopoda, Loliginidae). Zool Sci 22:645–651CrossRefGoogle Scholar

Copyright information

© Japanese Society of Fisheries Science 2018

Authors and Affiliations

  1. 1.Institute of Molecular MedicineNational Tsing Hua UniversityHsinchuTaiwan
  2. 2.Institute of Marine Affairs and Resource ManagementNational Taiwan Ocean UniversityKeelungTaiwan
  3. 3.Institute of Systems NeuroscienceNational Tsing Hua UniversityHsinchuTaiwan
  4. 4.Department of Life ScienceNational Tsing Hua UniversityHsinchuTaiwan

Personalised recommendations