Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Linking male and female morphology to reproductive success in captive southern calamary (Sepioteuthis australis)

L. M. van Camp A B E , P. G. Fairweather A , M. A. Steer C , S. C. Donnellan B and J. N. Havenhand D
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia.

B Evolutionary Biology Unit and Centre for Evolutionary Biology and Biodiversity, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.

C South Australian Research and Development Institute, PO Box 120, Henley Beach, SA 5022, Australia.

D Department of Marine Ecology, Tjärnö Marine Biological Laboratory, Göteborg University, 452 96 Strömstad, Sweden.

E Corresponding author. Email: lissa.vancamp@halliburton.com

Marine and Freshwater Research 56(7) 933-941 https://doi.org/10.1071/MF04287
Submitted: 23 November 2004  Accepted: 1 June 2005   Published: 14 October 2005

Abstract

Sexual selection theory predicts that mating success influences the evolution of traits. Previous behavioural observations of male Sepioteuthis australis have revealed two main mating strategies in the field: (1) large dominant males pair and mate with females, which they defend from (2) smaller males attempting to mate using ‘sneaker’ tactics. The current study examined whether fertilisation of squid eggs laid by polyandrous females within a mesocosm reflected this field-observed size-based mating system. Polymorphic microsatellite loci were used to identify mothers and fathers of embryos, which in turn allowed us to determine the effect of body size, age, and nine other morphological traits on reproductive success. Parentage of 112 embryos was assigned among 14 possible females and 20 candidate males of varying sizes. The mating behaviour observed in captivity was consistent with the size-based strategies seen in the field yet large males did not sire proportionally more offspring; instead nearly all males, regardless of size, sired some offspring. Regression analyses indicated that females did not select sperm based on male size, shape or age. Surprisingly, female contributions were skewed, with younger females contributing more eggs than older females. The possibility of male mate-choice was explored.

Extra keywords: cephalopod, mate choice, microsatellites, morphometrics, parentage, selection, squid.


Acknowledgments

We thank W. Hutchinson at SARDI for providing tank space, K. Saint and K. Ottewell for valuable practical discussion and advice, and A. Dyer for his constructive advice on the manuscript. This work was supported by the Australian Research Council (awarded to JNH) and Flinders Institute of Research in Science and Technology (awarded to PGF).


References

Andersson M. B. (1994). ‘Sexual Selection.’ (Princeton University Press: Princeton, NJ.)

Bateman, A. J. (1948). Intrasexual selection in Drosophila. Heredity 2, 349–368.
Forsythe J. W. (1993). A working hypothesis of how seasonal temperature change may impact the field growth of young cephalopods. In ‘Recent Advances in Cephalopod Fisheries Biology’. (Eds T. Okutani, R. O’Dor and T. Kubodera.) pp. 133–143. (Tokai University Press: Tokyo.)

Forsythe, J. W. (2004). Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Marine and Freshwater Research 55, 331–339.
Crossref | GoogleScholarGoogle Scholar | Hanlon R. T., and Messenger J. B. (1996). ‘Cephalopod Behaviour.’ (Cambridge University Press: Cambridge, MA.)

Hanlon, R. T. , and Wolterding, M. R. (1989). Behaviour, body patterning, growth and life history of Ocotpus briareus cultured in the laboratory. American Malacological Bulletin 7, 21–45.
Jantzen T. M. (2002). Reproductive biology of the southern calamary Sepioteuthis australis from South Australia: behaviour and morphometric analysis. Ph.D. Thesis, Flinders University, Adelaide.

Jantzen, T. M. , and Havenhand, J. N. (2002). Field observations of mating behaviour in the squid Sepioteuthis australis in South Australia. Bulletin of Marine Science 71, 1073–1080.


Jantzen, T. M. , and Havenhand, J. N. (2003a). Reproductive behaviour in the squid Sepioteuthis australis from South Australia: interactions on the spawning grounds. The Biological Bulletin 204, 305–317.
PubMed |

Jantzen, T. M. , and Havenhand, J. N. (2003b). Reproductive behavior in the squid Sepioteuthis australis from South Australia: ethogram of reproductive body patterns. The Biological Bulletin 204, 290–304.
PubMed |

Jaroensutasinee, M. , and Jaroensutasinee, K. (2003). Male body size influences female choice and male-male competition in the fiddler crab, Uca paradussumieri Bott, 1973 (Decapoda, Brachyura, Ocypodidae). Crustacean Research 76, 177–186.
Crossref | GoogleScholarGoogle Scholar |

Jennions, M. D. , and Petrie, M. (2000). Why do females mate multiply? A review of the genetic benefits. Biological Reviews 75, 21–64.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Jones, A. G. (2002). The evolution of alternative cryptic female choice strategies in age-structured populations. Evolution 56, 2530–2536.
PubMed |

Kassahn, K. S. , Donnellan, S. C. , Fowler, A. J. , Hall, K. C. , Adams, M. , and Shaw, P. W. (2003). Molecular and morphological analyses of the cuttlefish Sepia apama indicate a complex population structure. Marine Biology 143, 947–962.
Crossref | GoogleScholarGoogle Scholar |

LeBas, N. R. (2001). Microsatellite determination of male reproductive success in a natural population of the territorial ornate dragon lizard, Ctenophorus ornatus. Molecular Ecology 10, 193–203.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Levitan, D. R. (2004). Density-dependent sexual selection in external fertilizers: variances in male and female fertilization success along the continuum from sperm limitation to sexual conflict in the sea urchin Strongylocentrotus franciscanus. American Naturalist 164, 298–309.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Manning, T. J. (1985). Choosy females and correlates of male age. Journal of Theoretical Biology 116, 349–354.


Marshall, T. C. , Slate, J. , Kruuk, L. E. B. , and Pemberton, J. M. (1998). Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology 7, 639–655.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Miller, S. A. , Dykes, D. D. , and Polesky, H. F. (1988). A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Research 16, 1215..
PubMed |

Moltschaniwskyj, N. A. , and Martinez, P. (1998). Effects of temperature and food levels on the growth and condition of juvenile Sepia elliptica (Hoyle 1885): an experimental approach. Journal of Experimental Marine Biology and Ecology 229, 289–302.
Crossref | GoogleScholarGoogle Scholar |

Naud, M.-J. , Hanlon, R. T. , Hall, K. C. , Shaw, P. W. , and Havenhand, J. N. (2004). Behavioural and genetic assessment of reproductive success in a spawning aggregation of the Australian giant cuttlefish, Sepia apama. Animal Behaviour 67, 1043–1050.
Crossref | GoogleScholarGoogle Scholar |

Pecl, G. T. (2001). Flexible spawning strategies in tropical and temperate Sepioteuthis squids. Marine Biology 138, 93–101.
Crossref | GoogleScholarGoogle Scholar |

Pecl, G. T. (2004). The in situ relationships between season of hatching, growth and condition in the southern calamary, Sepioteuthis australis. Marine and Freshwater Research 55, 429–438.
Crossref | GoogleScholarGoogle Scholar |

Pecl, G. T. , Moltschaniwskyj, N. A. , Tracey, S. R. , and Jordan, A. R. (2004). Inter-annual plasticity of squid life history and population structure: ecological and management implications. Oecologia 139, 515–524.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Pitcher, T. E. , Neff, B. D. , Rodd, F. H. , and Rowe, L. (2003). Multiple mating and sequential mate choice in guppies: females trade up. Proceedings of the Royal Society of London. Series B. Biological Sciences 270, 1623–1629.
Crossref | GoogleScholarGoogle Scholar |

Raymond, M. , and Rousset, F. (1995). Genepop (version 1.2): population genetics software for exact tests and ecumenicism. The Journal of Heredity 86, 248–249.


Shaw, P. W. , and Boyle, P. R. (1997). Multiple paternity within the brood of single females of Loligo forbesi (Cephalopoda: Loliginidae), demonstrated with microsatellite DNA markers. Marine Ecology Progress Series 160, 279–282.


Shaw, P. W. , and Sauer, W. H. H. (2004). Multiple paternity and complex fertilisation dynamics in the squid Loligo vulgaris reynaudii. Marine Ecology Progress Series 270, 173–179.


Slate, J. , Marshall, T. C. , and Pemberton, J. (2000). A retrospective assessment of the accuracy of the paternity inference program cervus. Molecular Ecology 9, 801–808.
Crossref | cervus
.&journal=Molecular Ecology&volume=9&pages=801-808&publication_year=2000&author=J%2E%20Slate&hl=en&doi=10.1046/J.1365-294X.2000.00930.X" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar | PubMed |

Steer, M. A. , Moltschaniwskyj, N. A. , and Jordan, A. R. (2003). Embryonic development of southern calamary (Sepioteuthis australis) within the constraints of an aggregated egg mass. Marine and Freshwater Research 54, 217–226.
Crossref | GoogleScholarGoogle Scholar |

Thiel, M. , and Hinojosa, I. A. (2003). Mating behavior of female rock shrimp Rhynchocinetes typus (Decapoda: Caridea)—indication for convenience polyandry and cryptic female choice. Behavioural Ecology and Sociobiology 55, 113–121.
Crossref | GoogleScholarGoogle Scholar |

Tregenza, T. , and Wedell, N. (2000). Genetic compatibility, mate choice and patterns of parentage: invited Review. Molecular Ecology 9, 1013–1027.
Crossref | GoogleScholarGoogle Scholar | PubMed |

Václav, R. , and Hoi, H. (2002). Different reproductive tactics in house sparrows signalled by badge size: is there a benefit to being average? Ethology 108, 569–582.
Crossref | GoogleScholarGoogle Scholar |

van Camp, L. M. , Saint, K. S. , Donnellan, S. , Havenhand, J. N. , and Fairweather, P. G. (2003). Polymorphic microsatellite markers for paternity assessment in southern calamari Sepioteuthis australis (Cephalopoda: Loliginidae). Molecular Ecology Notes 3, 654–655.
Crossref | GoogleScholarGoogle Scholar |

van Camp, L. M. , Donnellan, S. C. , Dyer, A. R. , and Fairweather, P. G. (2004). Multiple paternity in field- and captive-laid egg strands of Sepioteuthis australis (Cephalopoda: Loliginidae). Marine and Freshwater Research 55, 819–823.
Crossref | GoogleScholarGoogle Scholar |

Wada, T. , Takegaki, T. , Mori, T. , and Natsukari, Y. (2005). Sperm displacement behaviour by the cuttlefish Sepia esculenta (Cephalopoda: Sepiidae). Journal of Ethology 23, 85–92.
Crossref | GoogleScholarGoogle Scholar |

Yasui, Y. (1998). The ‘genetic benefits’ of female multiple mating reconsidered. Trends in Ecology & Evolution 13, 246–250.
Crossref | GoogleScholarGoogle Scholar |

Zeh, J. A. , and Zeh, D. W. (1997). The evolution of polyandry II: post-copulatory defenses against genetic incompatibility. Proceedings of the Royal Society of London. Series B. Biological Sciences 264, 69–75.
Crossref | GoogleScholarGoogle Scholar |