Sexual selection in the sea: female promiscuity and male sperm competition in squid

A project undertaken at the Department of Zoology, University of Melbourne, and supervised by Dr Devi Stuart-Fox

Sexual selection accounts for much of the weird and wonderful diversity of life on earth - from the iconic peacock's train to sexual cannibalism in preying mantises. The full spectrum of this diversity is represented in a single group of animals: the cephalopods (cuttlefish, squids and octopuses). Cephalopods exhibit a bewildering array of reproductive behaviours and adaptations, from complex, technicoloured courtship displays to elaborate sperm storage structures, sperm removal devices and even sexual cannibalism.

All cephalopod species that have been studied mate with multiple partners, despite the presence of potentially costly reproductive behaviours. We examined the costs and benefits to female dumpling squid of mating with multiple males, and whether male dumpling squid experience any mating costs. Dumpling squid are small, short-lived and common in coastal waters along the coast of south eastern Australia.

We have documented the first evidence that females benefit from polyandry (mating with two or more different males) in any cephalopod. Females that mate with two different males produce clutches of eggs faster (less time between successive clutches) than females that mate with only one male. This is likely to give polyandrous females a reproductive advantage given that dumpling squid are short-lived and very vulnerable to predators. This benefit is also likely to compensate for the high costs of mating in this species.

Dumpling squid experience several costs of mating and exhibit costly mating behaviours (dumpling squid will mate, even in the presence of a fish predator!). After mating, dumpling squid have substantially reduced swimming ability, suggesting an energetic cost of mating. Even though an energetic mating cost sounds intuitive, it has rarely been demonstrated. In another experiment, we found that once mated female dumpling squid lived shorter lives than virgin dumpling squid. There was an even greater reduction in lifespan for females that were mated twice. Despite these costs, our research has shown that females lay eggs with up to four male sires. This suggests that the benefits mentioned above may outweigh these costs, or that there is a conflict between males and females in the optimal number of partners.

Male dumpling squid may have tactics to maximise the number of eggs his sperm fertilises. However, we found that the last male to mate with a female will fertilise the greatest number of her eggs. Dumpling squid can mate for up to three hours, despite the male transferring his sperm bundle to the female within the first 5 minutes. Holding on to the female for so long may be a tactic males use to stop the female mating with other males and increase his chances of being the last male to mate with her. 

Collaborators: Dr Mark Norman (Museum Victoria) and Dr. Bob Wong (Monash University)

Publications

Franklin, A. M. and Stuart-Fox, D. 2017. Single and multiple mating reduces longevity of female dumpling squid (Euprymna tasmanica). J. Evol. Biol. In press

Squires, Z. E., Wong, B. B. M., Norman, M. D. and Stuart-Fox, D. 2015. Last male sperm precedence in a polygamous squid.  Biological Journal of the Linnean Society 116(2): 277-287. doi: 10.1111/bij.12590

Franklin, A.M., Squires, Z.E. and Stuart-Fox, D. 2014. Does predation risk affect mating behaviour? An experimental test in squid.  PLoS One 9(12): e115027. doi: 10.1371/journal.pone.0115027

Squires, Z. E., Wong, B. B. M., Norman, M. D. and Stuart-Fox, D. 2014. Multiple paternity but no evidence of biased sperm use in female dumpling squid, Euprymna tasmanica. Marine Ecology Progress Series 511: 93-103. doi: 10.3354/meps10898

Squires ZE, Norman MD, Stuart-Fox D. 2013. Mating behaviour and general spawning patterns of the bobtail squid, Euprymna tasmanica: a laboratory study. Journal of Molluscan Studies 79(3): 263–269. doi: 10.1093/mollus/eyt025

Franklin, A.M., Squires, Z.E. and Stuart-Fox, D. 2012. The energetic cost of mating in a promiscuous cephalopod. Biology Letters 8: 754-756. doi: 10.1098/rsbl.2012.0556

Squires ZE, Wong BBM, Norman MD, Stuart-Fox D. 2012. Multiple fitness benefits of polyandry in a cephalopod. PLoS ONE 7(5): e37074. doi:10.1371/journal.pone.0037074

 
Figure 1. The Southern Dumpling Squid, Euprymna tasmanica, horizontal view. (Image by Mark Norman)

Figure 2. A mating pair of Southern Dumpling Squid. (Image by Mark Norman)

Figure 3. A Southern Dumpling Squid showing the'arm flower display'. (Image by Mark Norman)

Figure 4. Highly modified suckers on the left dorsal arm of mature males of the Southern Dumpling Squid, potentially used to displace the sperm packets of rivals. (Scanning electron micrograph by Mark Norman).

 

Figure 5. The average number of days between clutches laid by females that have mated with one male (monandry1), the same male twice (monandry2) and two different males (polyandry). Different letters show significantly different groups