Abstract
Conspicuous male sexual traits (e.g. weapons for male–male competition and displays for courting females) may attract predators. Under conditions of high predation risk, females typically become less choosy with respect to mates to reduce the time spent on mate selection. However, post-copulatory sexual traits, such as sperm ejaculation for sperm competition and sperm removal for cryptic female choice (CFC), may increase with predation risk because they are more inconspicuous to predators. To examine this hypothesis, we observed the reproductive behaviour in the Japanese pygmy squid, Idiosepius paradoxus, in which the male attaches ejaculated spermatangia to the female’s body and the female removes the spermatangia after copulation. Squid from two populations (Ohmura and Oki), with low and high predation levels, respectively, were copulated in tanks under controlled presence/absence of predator conditions. Among the Ohmura individuals, spermatangia removal was suppressed in the presence of a predator. Females may not be able to remove spermatangia effectively when facing a predator because they feel threatened by the predator; as a result, more spermatangia were retained during trials in which they were exposed to predators. In contrast, squid from the Oki (high predation) population, which is exposed to a higher predation risk, were not strongly affected by the predator presence. While the males ejaculated more spermatangia, the females removed more of them. The effect of sexual conflict may be greater than that of the predation risk in the pygmy squid. This suggests adaptive differences in post-copulatory sexual selection traits linked to predation.
Significance statement
In general, the strength of pre-copulatory sexual selection decreases with increasing predation risk because the sexual traits attract predators. However, post-copulatory sexual traits which are often inconspicuous may not be influenced by predation risk. Post-copulatory behaviour of Japanese pygmy squid collected from two populations experiencing different predation levels were investigated under experimental predator presence/absence conditions. Among low predations, individual sperm rejection by females (a post-copulatory trait) was suppressed in the presence of a predator. In contrast, individuals from the high predation population reported no change in sperm rejection. As with pre-copulatory sexual selection, post-copulatory female choice was suppressed by predator presence among individuals from a low predation. However, post-copulatory female choice was not affected by predator presence among individuals from the high-predation population. This may indicate predation-driven adaptive differences and plastic responses in post-copulatory traits.
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References
Andersson MB (1994) Sexual selection. Princeton University press. In: Princeton
Arnqvist G, Rowe L (2005) Sexual conflict. Princeton University press. In: Princeton
Bierbach D, Schulte M, Herrmann N, Tobler M, Stadler S, Jung CT, Kunkel B, Riesch R, Klaus S, Ziege M, Indy JR, Rodriguez LA, Plath M (2011) Predator-induced changes of female mating preferences: innate and experiential effects. BMC Evol Biol 11:190
Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic Press, San Diego
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135
Brodeur RD, Pearcy WG (1984) Food habits and dietary overlap of some shelf rockfishes (genus Sebastes) from the northeastern Pacific Ocean. Fish Bull 82:269–293
Crawley MJ (2005) Statistics: An Introduction Using R. John Wiley & Sons, West Sussex
Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University press, Princeton
Elgee KE, Evans JP, Ramnarine IW, Rush SA, Pitcher TE (2010) Geographic variation in sperm traits reflects predation risk and natural rates of multiple paternity in the guppy. J Evol Biol 23:1331–1338
Forsgren E (1992) Predation risk affects mate choice in a gobiid fish. Am Nat 140:1041–1049
Franklin AM, Squires ZE, Stuart-Fox D (2014) Does predation risk affect mating behavior? An experimental test in dumpling squid (Euprymna tasmanica). PLoS One 9:e115027
Garcia-Gonzalez F, Yasui Y, Evans JP (2015) Mating portfolios: bet-hedging, sexual selection and female multiple mating. Proc R Soc Biol Sci B 282:20141525
Godin JGJ, Briggs SE (1996) Female mate choice under predation risk in the guppy. Anim Behav 51:117–130
Hanlon RT, Messenger JB (1998) Cephalopod behaviour. Cambridge University Press, Cambridge
Hedrick AV, Dill LM (1993) Mate choice by female crickets is influenced by predation risk. Anim Behav 46:193–196
Horinouchi M, Sano M (2000) Food habits of fishes in a Zostera marina bed at Aburatsubo, Central Japan. Ichthyol Res 47:163–173
Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64
Johnson JB, Basolo AL (2003) Predator exposure alters female mate choice in the green swordtail. Behav Ecol 14:619–625
Karino K, Kuwamura T, Nakashima Y, Sakai Y (2000) Predation risk and the opportunity for female mate choice in a coral reef fish. J Ethol 18:109–114
Kasugai T (2000) Reproductive behavior of the pygmy cuttlefish Idiosepius paradoxus in an aquarium. Venus 59:37–44
Kelly CD, Godin JGJ (2001) Predation risk reduces male-male sexual competition in the Trinidadian guppy (Poecilia reticulata). Behav Ecol Sociobiol 51:95–100
Kim TW, Christy JH, Dennenmoser S, Choe JC (2009) The strength of a female mate preference increases with predation risk. Proc R Soc Biol Sci B. 276:775–780
Kwak SN, Baeck GW, Klumpp DW (2005) Comparative feeding ecology of two sympatric greenling species, Hexagrammos otakii and Hexagrammos agrammus in eelgrass Zostera marina beds. Environ Biol Fish 74:129–140
Lima SL, Dill LM (1990) Behavioral decisions made under the risk of predation: a review and prospectus. Can J Zool 68:619–640
Lodé T, Holveck MJ, Lesbarrères D, Pagano A (2004) Sex–biased predation by polecats influences the mating system of frogs. Proc R Soc Biol Sci B. 271:S399–S401
Lu CC, Dunning MC (1998) Subclass Coleoidea. In: Beesley PL, GJB R, Wells A (eds) Mollusca: the Southern Synthesis. Fauna of Australia, 5. Part A. CSIRO publishing, Melbourne, pp 499–563
Magnhagen C (1991) Predation risk as a cost of reproduction. Trends Ecol Evol 6:183–186
Maier G, Berger I, Burghard W, Nassal B (2000) Is mating of copepods associated with increased risk of predation? J Plankton Res 22:1977–1987
Michalska K (2016) The effect of predation risk on spermatophore deposition rate of the eriophyoid mite, Aculops allotrichus. Exp Appl Acarol 68:145–154
Neff BD, Pitcher TE, Ramnarine IW (2008) Inter-population variation in multiple paternity and reproductive skew in the guppy. Mol Ecol 17:2975–2984
Nishiumi N, Mori A (2015) Distance-dependent switching of anti-predator behavior of frogs from immobility to fleeing. J Ethol 33:117–124
Pitcher TE, Doucet SM, Beausoleil JM, Hanley D (2009) Secondary sexual characters and sperm traits in coho salmon Oncorhynchus kisutch. J Fish Biol 74:1450–1461
R Development Core Team (2017) R: A language and environment for statistical computing, reference index version 3.4.2. R Foundation for Statistical Computing, Vienna, Austria www.R-project.org
Sano M (1998) Is recruitment of the temperate sand goby, Sagamia geneionema, affected by habitat patch characteristics? Ichthyol Res 45:13–18
Sasaki M (1923) On an adhering habit of a pygmy cuttlefish, Idiosepius pygmaeus steenstrup. Annot Zool Jpn 10:209–213
Sato N (2017) Seasonal changes in reproductive traits and paternity in the Japanese pygmy squid Idiosepius paradoxus. Mar Ecol Prog Ser 582:121–131
Sato N, Kasugai T, Ikeda Y, Munehara H (2010) Structure of the seminal receptacle and sperm storage in the Japanese pygmy squid. J Zool 282:151–156
Sato N, Yoshida MA, Fujiwara E, Kasugai T (2013a) High-speed camera observations of copulatory behaviour in Idiosepius paradoxus: function of the dimorphic hectocotyli. J Mollus Stud 79:183–186
Sato N, Kasugai T, Munehara H (2013b) Sperm transfer or spermatangia removal: postcopulatory behaviour of picking up spermatangium by female Japanese pygmy squid. Mar Biol 160:553–561
Sato N, Kasugai T, Munehara H (2014a) Spermatangium formation and sperm discharge in the Japanese pygmy squid Idiosepius paradoxus. Zoology 117:192–199
Sato N, Kasugai T, Munehara H (2014b) Female pygmy squid cryptically favour small males and fast copulation as observed by removal of spermatangia. Evol Biol 41:221–228
Sato N, Yoshida MA, Kasugai T (2017) Impact of cryptic female choice on insemination success: larger sized and longer copulating male squid ejaculate more, but females influence insemination success by removing spermatangia. Evolution 71:111–120
Simmons LW, Emlen DJ (2006) Evolutionary trade-off between weapons and testes. Proc Nat Acad Sci 103:16346–16351
Stockley P, Gage MJG, Parker GA, Møller AP (1997) Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. Am Nat 149:933–954
Taylor AR, Persons MH, Rypstra AL (2005) The effect of perceived predation risk on male courtship and copulatory behavior in the wolf spider Pardosa milvina (Araneae, Lycosidae). J Arachnol 33:76–81
Thornhill R (1983) Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am Nat 122:765–788
Willis PM, Rosenthal GG, Ryan MJ (2012) An indirect cue of predation risk counteracts female preference for conspecifics in a naturally hybridizing fish Xiphophorus birchmanni. PLoS One 7:e34802
Yamane T, Okada K, Nakayama S, Miyatake T (2010) Dispersal and ejaculatory strategies associated with exaggeration of weapon in an armed beetle. Proc R Soc Biol Sci B 277:1705–1710
Acknowledgements
We thank Dr. S. Awata and Dr. N. Hirohashi for supporting specimen collection and Dr. N. J. McKeown for their critical comments on the manuscript. We thank an associate editor, Dr. D. J. Hosken and three referees for their helpful comments. This research was supported financially by Research Fellowships of the Japan Society for the Promotion of Science for Young Scientists (to NS). The author (NS) also thanks the faculty of Life and Environmental Science in Shimane University for help in financial support for publishing this report.
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This study was approved by the Animal Care and Use Committee of Faculty of Fisheries, Nagasaki University (permission no. NF-0014), in accordance with the Guidelines for Animal Experimentation of Faculty of Fisheries (fish, amphibians and invertebrates), and Regulations of the Animal Care and Use Committee, Nagasaki University.
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Sato, N., Uchida, Y. & Takegaki, T. The effect of predation risk on post-copulatory sexual selection in the Japanese pygmy squid. Behav Ecol Sociobiol 72, 129 (2018). https://doi.org/10.1007/s00265-018-2540-4
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DOI: https://doi.org/10.1007/s00265-018-2540-4