Skip to main content

Dimorphic male squid show differential gonadal and ejaculate expenditure

Abstract

Under intense sexual selection, males less successful in fighting and mate guarding often adopt alternative reproductive tactics. In many species, males employing alternative tactics show not only behavioral differences, but also divergences in morphology and physiology, a phenomenon called intrasexual male dimorphism. Herein, we investigated intrasexual male dimorphism in the loliginid squid Doryteuthis plei, associated with alternative mating tactics. We show that small males (sneakers) have spermatophores with discontinuously smaller sperm mass and longer spermatozoa than large males (consorts). Moreover, sneakers produce club-like spermatangia, whereas consorts produce hook-like spermatangia, each type of spermatangia associated with a different female storage site and adoption of a distinct mating position. We also show that dimorphic males have different gonadal investment, sneakers showing higher increment rates in testis mass and higher investment in spermatophoric complex than consorts. Under the complex squid mating system, with two distinct fertilization environments, we hypothesize that sneakers may maximize their reproductive success by both investing more in gonad growth and partitioning ejaculates into extra mating opportunities, whereas consorts may benefit from investment in somatic growth. Squids may be the first example of animals that, even with distinct sperm storage sites, fit the general predictions of sneaks and guards theoretical models.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Alonzo, S. H. & R. R. Warner, 2000. Allocation to mate guarding or increased sperm production in a Mediterranean wrasse. The American Naturalist 156: 266–275.

    Article  Google Scholar 

  • Andersson, M., 1994. Sexual Selection. Princeton University Press, Princeton.

    Google Scholar 

  • Ball, M. A. & G. A. Parker, 1996. Sperm competition games: external fertilization and “adaptive” infertility. Journal of Theoretical Biology 180: 141–150.

    CAS  Article  PubMed  Google Scholar 

  • Bates, D., M. Machler, B. M. Bolker & S. C. Walker, 2005. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67: 1–48.

    Google Scholar 

  • Boletzky, S. V., 1986. Encapsulation of cephalopod embryos: a search for functional correlations. American Malacological Bulletin 4: 217–227.

    Google Scholar 

  • Bonduriansky, R., 2007. Sexual selection and allometry: a critical reappraisal of the evidence and ideas. Evolution 61: 838–849.

    Article  PubMed  Google Scholar 

  • Briskie, J. V. & R. Montgomerie, 1992. Sperm size and sperm competition in birds. Proceedings of the Royal Society of London B: Biological Sciences 247: 89–95.

    CAS  Article  Google Scholar 

  • Briskie, J. V., R. Montgomerie & T. R. Birkhead, 1997. The evolution of sperm size in birds. Evolution 51: 937–945.

    Article  PubMed  Google Scholar 

  • Buresch, K. M., R. T. Hanlon, M. R. Maxwell & S. Ring, 2001. Microsatellite DNA markers indicate a high frequency of multiple paternity within individual field-collected egg capsules of the squid Loligo pealeii. Marine Ecology Progress Series 210: 161–165.

    Article  Google Scholar 

  • Buresch, K. C., M. R. Maxwell, M. R. Cox & R. T. Hanlon, 2009. Temporal dynamics of mating and paternity in the squid Loligo pealeii. Marine Ecology Progresss Series 387: 197–203.

    Article  Google Scholar 

  • Byrne, P. G., L. W. Simmons & J. D. Roberts, 2003. Sperm competition and the evolution of gamete morphology in frogs. Proceedings of the Royal Society of London B: Biological Sciences 270: 2079–2086.

    Article  Google Scholar 

  • Cornwallis, C. K. & T. R. Birkhead, 2006. Social status and availability of females determine patterns of sperm allocation in the fowl. Evolution 60: 1486–1493.

    Article  PubMed  Google Scholar 

  • Dewsbury, D. A., 1982. Ejaculate cost and mate choice. The American Naturalist 119: 601–610.

    Article  Google Scholar 

  • DiMarco, F. P. & R. T. Hanlon, 1997. Agonistic behavior in the squid Loligo plei (Loliginidae, Teuthoidea): Fighting tactics and the effects of size and resource value. Ethology 103: 89–108.

    Article  Google Scholar 

  • Dominey, W. J., 1980. Female mimicry in male bluegill sunfish - a genetic polymorphism? Nature 284: 546–548.

    Article  Google Scholar 

  • Drew, G. A., 1919. Sexual activities of the squid, Loligo pealii. II. The spermatophore; its structure, ejaculation and formation. Journal of Morphology 32: 379–435.

    Article  Google Scholar 

  • Dybas, L. K. & H. S. Dybas, 1981. Coadaptation and taxonomic differentiation of sperm and spermathecae in featherwing beetles. Evolution 35: 168–174.

    Article  PubMed  Google Scholar 

  • Eberhard, W. G. & E. E. Gutiérrez, 1991. Male dimorphisms in beetles and earwigs and the question of developmental constraints. Evolution 45: 18–28.

    Article  PubMed  Google Scholar 

  • Emlen, D. J., 1997. Alternative reproductive tactics and male-dimorphism in the horned beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Behavioral Ecology and Sociobiology 41: 335–341.

    Article  Google Scholar 

  • Farrell, L. L., T. Burke, J. Slate, S. B. McRae & D. B. Lank, 2013. Genetic mapping of the female mimic morph locus in the ruff. BMC Genetics 14: 1–4.

    Article  Google Scholar 

  • Fields, W. G., 1965. The structure, development, food relations, reproduction, and life history of the squid Loligo opalescens Berry. Fisheries Bulletin 131: 1–108.

    Google Scholar 

  • Gadgil, M., 1972. Male dimorphism as a consequence of sexual selection. The American Naturalist 106: 574–580.

    Article  Google Scholar 

  • Gage, M. J. G., 1994. Associations between body size, mating pattern, testis size and sperm lengths across butterflies. Proceedings of the Royal Society of London B: Biological Sciences 258: 247–254.

    Article  Google Scholar 

  • Gage, M. J. G. & R. P. Freckleton, 2003. Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proceedings of the Royal Society of London B: Biological Sciences 270: 625–632.

    Article  Google Scholar 

  • Gage, M. J. G. & E. H. Morrow, 2003. Experimental evidence for the evolution of numerous, tiny sperm via sperm competition. Current Biology 13: 754–757.

    CAS  Article  PubMed  Google Scholar 

  • Gage, M. J. G., P. Stockley & G. A. Parker, 1995. Effects of alternative male mating strategies on characteristics of sperm production in the Atlantic salmon (Salmo salar): theoretical and empirical investigations. Philosophical Transactions of the Royal Society B: Biological Sciences 350: 391–399.

    Article  Google Scholar 

  • Gomendio, M. & E. R. S. Roldan, 1991. Sperm competition influences sperm size in mammals. Proceedings of the Royal Society of London B: Biological Sciences 243: 181–185.

    CAS  Article  Google Scholar 

  • Gomendio, M. & E. R. S. Roldan, 1993. Coevolution between male ejaculates and female reproductive biology in eutherian mammals. Proceedings of the Royal Society of London B: Biological Sciences 252: 7–12.

    CAS  Article  Google Scholar 

  • Gross, M. R., 1996. Alternative reproductive strategies and tactics: diversity within sexes. Trends in Ecology & Evolution 11: 92–98.

    CAS  Article  Google Scholar 

  • Gross, M. R. & J. Repka, 1998. Stability with inheritance in the conditional strategy. Journal of Theoretical Biology 192: 445–453.

    CAS  Article  PubMed  Google Scholar 

  • Hanlon, R. T., 1996. Evolutionary games that squids play: fighting, courting, sneaking, and mating behaviors used for sexual selection in Loligo pealei. Biological Bulletin 191: 309–310.

    CAS  Article  PubMed  Google Scholar 

  • Hanlon, R. T., 1998. Mating systems and sexual selection in the squid Loligo: How might commercial fishing on spawning squids affect them? California Cooperative Oceanic Fisheries Investigations Reports 39: 92–100.

    Google Scholar 

  • Hanlon, R. T. & J. B. Messenger, 1996. Cephalopod Behaviour. Cambridge University Press, Cambridge.

    Google Scholar 

  • Hanlon, R. T., M. R. Maxwell & N. Shashar, 1997. Behavioral dynamics that would lead to multiple paternity within egg capsules of the squid Loligo pealei. Biological Bulletin 193: 212–214.

    CAS  Article  PubMed  Google Scholar 

  • Hanlon, R. T., M. J. Smale & W. H. H. Sauer, 2002. The mating system of the squid Loligo vulgaris reynaudii (Cephalopoda, Mollusca) off South Africa: fighting, guarding, sneaking, mating and egg laying behavior. Bulletin of Marine Science 71: 331–345.

    Google Scholar 

  • Hazel, W. N., R. Smock & M. D. Johnson, 1990. A polygenic model for the evolution and maintenance of conditional strategies. Proceedings of the Royal Society of London B: Biological Sciences 242: 181–187.

    CAS  Article  Google Scholar 

  • Hazel, W. N., R. Smock & C. M. Lively, 2004. The ecological genetics of conditional strategies. The American Naturalist 163: 888–900.

    Article  PubMed  Google Scholar 

  • Hirohashi, N. & Y. Iwata, 2013. The different types of sperm morphology and behavior within a single species: Why do sperm of squid sneaker males form a cluster? Comunicative & Integrative Biology 6: e26729.

    Article  Google Scholar 

  • Hirohashi, N., L. Alvarez, K. Shiba, E. Fujiwata, Y. Iwata, T. Mohri, K. Inaba, K. Chiba, H. Ochi, C. T. Supuran, N. Kotzur, Y. Kakiuchi, U. B. Kaupp & S. A. Baba, 2013. Sperm from sneaker male squids exhibit chemotactic swarming to CO2. Current Biology 23: 1–7.

    Article  Google Scholar 

  • Hirohashi, N., M. Tamura-Nakano, F. Nakaya, T. Iida & Y. Iwata, 2016. Sneaker male squid produce long-lived spermatozoa by modulating their energy metabolism. The Journal of Biological Chemistry: jbc-M116.

  • Hosken, D. J., 1997. Sperm competition in bats. Proceedings of the Royal Society of London B: Biological Sciences 264: 385–392.

    CAS  Article  Google Scholar 

  • Hunt, J. & L. W. Simmons, 2001. Status-dependent selection in the dimorphic beetle Onthophagus taurus. Proceedings of the Royal Society of London B: Biological Sciences 268: 2409–2414.

    CAS  Article  Google Scholar 

  • Immler, S. & T. R. Birkhead, 2007. Sperm competition and sperm midpiece size: no consistent pattern in passerine birds. Proceedings of the Royal Society of London B: Biological Sciences 274: 561–568.

    Article  Google Scholar 

  • Immler, S., S. Pitnick, G. A. Parker, K. L. Durrant, S. Lupold, S. Calhim & T. R. Birkhead, 2011. Resolving variation in the reproductive trade-off between sperm size and number. Proceedings of the National Academy of Sciences 108: 5325–5330.

    CAS  Article  Google Scholar 

  • Iwata, Y. & Y. Sakurai, 2007. Threshold dimorphism in ejaculate characteristics in the squid Loligo bleekeri. Marine Ecology Progress Series 345: 141–146.

    Article  Google Scholar 

  • Iwata, Y., H. Munehara & Y. Sakurai, 2005. Dependence of paternity rates on alternative reproductive behaviors in the squid Loligo bleekeri. Marine Ecology Progress Series 298: 219–228.

    Article  Google Scholar 

  • Iwata, Y., P. Shaw, E. Fujiwara, K. Shiba, Y. Kakiuchi & N. Hirohashi, 2011. Why small males have big sperm: dimorphic squid sperm linked to alternative mating behaviours. BMC Evolutionary Biology 11: 1–9.

    Article  Google Scholar 

  • Iwata, Y., Y. Sakurai & P. Shaw, 2015. Dimorphic sperm-transfer strategies and alternative mating tactics in loliginid squid. Journal of Molluscan Studies 81: 147–151.

    Article  Google Scholar 

  • LaMunyon, C. W. & S. Ward, 1998. Larger sperm outcompete smaller sperm in the nematode Caenorhabditis elegans. Proceedings of the Royal Society of London B: Biological Sciences 265: 1997–2002.

    CAS  Article  Google Scholar 

  • LaMunyon, C. W. & S. Ward, 1999. Evolution of sperm size in nematodes: sperm competition favours larger sperm. Proceedings of the Royal Society of London B: Biological Sciences 266: 263–267.

    CAS  Article  Google Scholar 

  • Lank, D. B., L. L. Farrell, T. Burke, T. Piersma & S. B. McBae, 2013. A dominant allele controls development into female mimic male and diminutive female ruffs. Biology Letters 9: 1–4.

    Article  Google Scholar 

  • Marian, J. E. A. R., 2012. Spermatophoric reaction reappraised: novel insights into the functioning of the loliginid spermatophore based on Doryteuthis plei (Mollusca: Cephalopoda). Journal of Morphology 273: 248–278.

    Article  PubMed  Google Scholar 

  • Mazzoldi, C., M. Scaggiante, E. Ambrosin & M. B. Rasotto, 2000. Mating system and alternative male mating tactics in the grass goby Zosterisessor ophiocephalus (Teleostei: Gobiidae). Marine Biology 137: 1041–1048.

    Article  Google Scholar 

  • Moltschaniwskyj, N. A., K. Hall, M. R. Lipinski, J. E. A. R. Marian, M. Nishiguchi, M. Sakai, D. J. Shulman, B. Sinclair, D. L. Sinn, M. Staudinger, R. Van Gelderen, R. Villanueva & K. Warnke, 2007. Ethical and welfare considerations when using cephalopods as experimental animals. Reviews in Fish Biology and Fisheries 17: 455–476.

    Article  Google Scholar 

  • Morrow, E. H. & M. J. G. Gage, 2000. The evolution of sperm length in moths. Proceedings of the Royal Society of London B: Biological Sciences 267: 307–313.

    CAS  Article  Google Scholar 

  • Olsson, M., T. Madsen & R. Shine, 1997. Is sperm really so cheap? Costs of reproduction in male adders, Vipera berus. Proceedings of the Royal Society of London B: Biological Sciences 264: 455–459.

    Article  Google Scholar 

  • Parker, G. A., 1970. Sperm competition and its evolutionary consequences in the insects. Biological Reviews 45: 525–567.

    Article  Google Scholar 

  • Parker, G. A., 1982. Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. Journal of Theoretical Biology 96: 281–294.

    CAS  Article  PubMed  Google Scholar 

  • Parker, G. A., 1990a. Sperm competition games: raffles and roles. Proceedings of the Royal Society of London B: Biological Sciences 242: 120–126.

    Article  Google Scholar 

  • Parker, G. A., 1990b. Sperm competition games: sneaks and extra-pair copulations. Proceedings of the Royal Society of London B: Biological Sciences 242: 127–133.

    Article  Google Scholar 

  • Parker, G. A., 1993. Sperm competition games: sperm size and sperm number under adult control. Proceedings of the Royal Society of London B: Biological Sciences 253: 245–254.

    CAS  Article  Google Scholar 

  • Parker, G. A., 1998. Sperm competition and the evolution of ejaculates: towards a theory base. In Birkhead, T. R. & A. P. Møller (eds), Sperm Competition and Sexual Selection. Academic Press, San Diego: 3–54.

    Chapter  Google Scholar 

  • Parker, G. A. & T. Pizzari, 2010. Sperm competition and ejaculate economics. Biological Reviews 85: 897–934.

    PubMed  Google Scholar 

  • Parker, G. A., M. A. Ball, P. Stockley & J. G. Gage, 1997. Sperm competition games: a prospective analysis of risk assessment. Proceedings of the Royal Society of London B: Biological Sciences 264: 1793–1802.

    CAS  Article  Google Scholar 

  • Parker, G. A., C. M. Lessells & L. W. Simmons, 2013. Sperm competition games: a general model for precopulatory male-male competition. Evolution 67: 95–109.

    Article  PubMed  Google Scholar 

  • Perez, J. A. A., D. C. Aguiar & U. C. Oliveira, 2002. Biology and population dynamics of the long-finned squid Loligo plei (Cephalopoda: Loliginidae) in southern Brazilian waters. Fisheries Research 58: 267–279.

    Article  Google Scholar 

  • Petrie, M., 1988. Intraspecific variation in structures that display competitive ability: large animals invest relatively more. Animal Behavior 36: 1174–1179.

    Article  Google Scholar 

  • Pitnick, S., 1996. Investments in testes and the cost of making long sperm in Drosophila. The American Naturalist 148: 57–80.

    Article  Google Scholar 

  • Postuma, F. A. & M. A. Gasalla, 2014. Reproductive activity of the tropical arrow squid Doryteuthis plei around São Sebastião Island (SE Brazil) based on a 10-year fisheries monitoring. Fisheries Research 152: 45–54.

    Article  Google Scholar 

  • R Development Core Team, 2008. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.

  • Radwan, J., 1996. Intraspecific variation in sperm competition success in the bulb mite: a role for sperm size. Proceedings of the Royal Society of London B: Biological Sciences 263: 855–859.

    Article  Google Scholar 

  • Rhen, T. & D. Crews, 2002. Variation in reproductive behavior within a sex: neural systems and endocrine activation. Journal of Neuroendocrinology 14: 517–531.

    CAS  Article  PubMed  Google Scholar 

  • Repka, J. & M. R. Gross, 1995. The evolutionarily stable strategy under individual condition and tactic frequency. Journal of Theoretical Biology 176: 27–31.

    CAS  Article  PubMed  Google Scholar 

  • Rudolfsen, G., L. Figenschou, I. Folstad, H. Tveiten & M. Figenschou, 2006. Rapid adjustments of sperm characteristics in relation to social status. Proceedings of the Royal Society of London B: Biological Sciences 273: 325–332.

    Article  Google Scholar 

  • Scaggiante, M., C. Mazzoldi, C. W. Petersen & M. B. Rasotto, 1999. Sperm competition and mode of fertilization in the grass goby Zosterisessor ophiocephalus (Teleostei: Gobiidae). Journal of Experimental Zoology 283: 81–90.

    Article  Google Scholar 

  • Shashar, N. & R. T. Hanlon, 2013. Spawning behavior dynamics at communal egg beds in the squid Doryteuthis (Loligo) pealeii. Journal of Experimental Marine Biology and Ecology 447: 65–74.

    Article  Google Scholar 

  • Shuster, S. M. & C. Sassaman, 1997. Genetic interaction between male mating strategy and sex ratio in a marine isopod. Nature 388: 373–377.

    CAS  Article  Google Scholar 

  • Shuster, S. M. & M. J. Wade, 2003. Mating systems and strategies. Princeton University Press, Princeton.

    Google Scholar 

  • Simmons, L. W. & D. J. Emlen, 2006. Evolutionary trade-off between weapons and testes. Proceedings of the National Academy of Sciences 103: 16346–16351.

    CAS  Article  Google Scholar 

  • Simmons, L. W., D. J. Emlen & J. L. Tomkins, 2007. Sperm competition games between sneakers and guards: a comparative analysis using dimorphic male beetles. Evolution 61: 2684–2692.

    Article  PubMed  Google Scholar 

  • Simmons, L. W., J. L. Tomkins & J. Hunt, 1999. Sperm competition games played by dimorphic male beetles. Proceedings of the Royal Society of London B: Biological Sciences 266(145): 150.

    Google Scholar 

  • Sinervo, B. & K. R. Zamudio, 2001. The evolution of alternative reproductive strategies: fitness differential, heritability, and genetic correlation between the sexes. The American Genetic Association 92: 198–205.

    CAS  Google Scholar 

  • Stern, D. L. & D. J. Emlen, 1999. The developmental basis for allometry in insects. Development 126: 1091–1101.

    CAS  PubMed  Google Scholar 

  • Stockley, P. & A. Purvis, 1993. Sperm competition in mammals: a comparative study of male roles and relative investment in sperm production. Functional Ecology 7: 560–570.

    Article  Google Scholar 

  • Stockley, P., M. J. G. Gage, G. A. Parker & A. P. Møller, 1997. Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. The American Naturalist 149: 933–954.

    CAS  Article  PubMed  Google Scholar 

  • Taborsky, M., 1994. Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Advances in the study of behavior 23: 1–100.

    Article  Google Scholar 

  • Taborsky, M., 1998. Sperm competition in fish: ‘bourgeois’ males and parasitic spawning. Trends in Ecology & Evolution 13: 222–227.

    CAS  Article  Google Scholar 

  • Taborsky, M., R. F. Oliveira & J. Brockmann, 2008. The evolution of alternative reproductive tactics: concepts and questions. In Oliveira, R. F., M. Taborsky & H. J. Brockmann (eds), Alternative Reproductive Tactics: An Integrative Approach. Cambridge University Press, Cambridge: 1–21.

    Google Scholar 

  • Tomkins, J. L. & L. W. Simmons, 2000. Sperm competition games played by dimorphic male beetles: fertilization gains with equal mating access. Proceedings of the Royal Society of London B: Biological Sciences 267: 1547–1553.

    CAS  Article  Google Scholar 

  • Tomkins, J. L. & L. W. Simmons, 2002. Measuring relative investment: a case study of testes investment in species with alternative male reproductive tactics. Animal Behaviour 63: 1009–1016.

    Article  Google Scholar 

  • Tomkins, J. L. & W. Hazel, 2007. The status of the conditional evolutionarily stable strategy. TRENDS in Ecology and Evolution 22: 522–528.

    Article  PubMed  Google Scholar 

  • Tomkins, J. L., J. S. Kotiaho & N. R. LeBas, 2005. Matters of scale: positive allometry and the evolution of male dimorphisms. The American Naturalist 165: 389–402.

    Article  PubMed  Google Scholar 

  • Warner, R. R., D. Y. Shapiro, A. Marcanato & C. W. Petersen, 1995. Sexual conflict: males with highest mating success convey the lowest fertilization benefits to females. Proceedings of the Royal Society of London B: Biological Sciences 262: 135–139.

    CAS  Article  Google Scholar 

  • Warton, D. I., I. J. Wright, D. S. Falster & M. Westoby, 2006. Bivariate line-fitting methods for allometry. Biological Reviews 81: 259–291.

    Article  PubMed  Google Scholar 

  • Warton, D. I., R. A. Duursma, D. S. Falster & S. Taskinen, 2012. SMATR 3 - an R package for estimation and inference about allometric lines. Methods in Ecology and Evolution 3: 257–259.

    Article  Google Scholar 

  • Wedell, N., M. J. G. Gage & G. A. Parker, 2002. Sperm competition, male prudence and sperm-limited females. Trends in Ecology & Evolution 17: 313–320.

    Article  Google Scholar 

  • Zeidberg, L. D., 2009. First observations of “sneaker mating” in the California market squid, Doryteuthis opalescens, (Cephalopoda: Myopsida). Marine Biodiversity Records 2: 1–4.

    Article  Google Scholar 

Download references

Acknowledgements

This study was conducted as part of the first author’s Master dissertation in the Graduate Program in Zoology of the Department of Zoology, at the University of São Paulo (USP). The authors appreciate the financial support and grants provided by CAPES (Coordination for the Improvement of Higher Education Personnel), CAPES/PROEX and CNPq (National Council for Scientific and Technological Development—Proc. 477233/2013-9). The authors are also grateful for the support from the following laboratories and institutions: “Centro de Biologia Marinha” (logistic support for animal collection and maintenance, light microscopy facilities), “Laboratório de Cultivo e Estudos de Cnidaria” (light microscopy facilities), “Laboratório de Entomologia e Aracnologia” (light microscopy facilities), and “Laboratório de Biologia Celular de Invertebrados Marinhos” (citocentrifuge facilities for spermatozoa preparation). The authors specially thank Dr. Alvaro E. Migotto, from “Centro de Biologia Marinha,” for the invaluable assistance during in vitro experimentation and digital filming of the spermatophoric reaction, Dr. Glauco Machado (USP) for his helpful critical reading of the research proposal, Dr. Bruno Buzatto (University of Southwestern Australia) for the inestimable assistance and critical comments concerning statistical analyses, and the colleagues at CIAC 2015 Symposium (Hakodate, Japan) for all comments and suggestions that helped to improve this study. Glauco Machado, Bruno Buzatto, Vlad Laptikhovsky, and an anonymous reviewer helped to improve the quality of the manuscript and are greatly appreciated. This is a contribution of NP-BioMar (Research Center for Marine Biodiversity, USP).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lígia H. Apostólico.

Additional information

Guest editors: Erica A. G. Vidal, Ian G. Gleadall & Natalie Moltschaniswskyi / Advances in Cephalopod Ecology and Life Cycles

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 3 Digital filming of in vitro experiment of spermatophoric reaction and hook-like spermatangium formation in a consort male (mantle length = 252.0 mm) of the squid Doryteuthis plei, conducted under a Zeiss SV-11 stereomicroscope coupled to a Sony NEX FS700 digital camera. The spermatophore was dissected from the spermatophoric sac of the anesthetized male and placed in a Petri dish filled with filtered seawater. The spermatophoric reaction was induced by rapidly pulling the cap thread, aided by dissecting forceps. The reaction encompasses a series of complex evagination processes of membranes and tunics of the spermatophore, resulting on the formation of a hook-like spermatangium (i.e., everted spermatophore containing the sperm mass). (WMV 26364 kb)

Online Resource 4 Digital filming of in vitro experiment of spermatophoric reaction and club-like spermatangium formation in a sneaker male (mantle length = 106.0 mm) of the squid Doryteuthis plei, conducted under a Zeiss SV-11 stereomicroscope coupled to a Sony NEX FS700 digital camera. The spermatophore was dissected from the spermatophoric sac of the anesthetized male and placed in a Petri dish filled with filtered seawater. The spermatophoric reaction was induced by rapidly pulling the cap thread, aided by dissecting forceps. The reaction encompasses a series of complex evagination processes of membranes and tunics of the spermatophore, resulting on the formation of a club-like spermatangium (i.e., everted spermatophore containing the sperm mass). (WMV 9283 kb)

10750_2017_3145_MOESM1_ESM.pdf

Online Resource 1 Detailed description of the regression model (and equations used), adapted from Eberhard & Gutierrez (1991) original article. This analysis was applied herein for the detection of a body-size switch point (i.e., detection of male intrasexual dimorphism) in the squid Doryteuthis plei. (PDF 104 kb)

10750_2017_3145_MOESM2_ESM.pdf

Online Resource 2 Results of the analysis for detection of male intrasexual dimorphism in Doryteuthis plei, based on the models described in Eberhard & Gutierrez (1991). Regression coefficients and significance tests for each model are provided. For spermatophore length, the best-fit switch point was at 220.2 mm of mantle length (Model 3, adjusted R 2 = 0.891); for sperm mass length, the best-fit switch point was at 215.1 mm of mantle length (Model 3, adjusted R 2 = 0.874); for sperm mass length index (SMLI), the best-fit switch point was at 169.3 mm of mantle length (Model 2, adjusted R 2 = 0.690); and for sperm mass volume, the best-fit switch point was at 205.0 mm of mantle length (Model 2, adjusted R 2 = 0.789). (PDF 142 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Apostólico, L.H., Marian, J.E.A.R. Dimorphic male squid show differential gonadal and ejaculate expenditure. Hydrobiologia 808, 5–22 (2018). https://doi.org/10.1007/s10750-017-3145-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-017-3145-z

Keywords

  • Allocation trade-off
  • Allometry
  • Alternative reproductive tactics
  • Conditional strategy
  • Intrasexual male dimorphism
  • Male–male competition
  • Sperm competition
  • Status dependence