Rushi Tawade
Drawing by Rushi Tawade
While looking at a dissected male market squid (Doryteuthis opalescens) in lab, one of the things that struck me most was the size of the testis. The single fused testis could clearly be seen as a long white mass occupying almost a third of this animal’s internal cavity (Fig. 1). I had seen large gonads in other mollusks, like bivalves, but those were sessile creatures that needed to produce huge amounts of sperm and eggs to even the odds of external fertilization in the waves. Male squid effectively inseminated females internally by transferring spermatophores via a modified tentacle; the hectocotylus. Why then did they need to produce so much sperm? What selective pressures could have led to so much of this squid’s internal cavity being dedicated solely to gamete production? I decided to explore the literature for answers, and ended up finding out quite a bit about squid mating systems.
Photo by Peter Brueggeman, source: http://www.peterbrueggeman.com/photos/2011dec6.htm
Like other Loliginid squid, cohorts of Market Squid along the California coast migrate inshore at around eleven months of age and form large mixed-sex schools in shallow waters to spawn (dying soon after; Fig. 2). Mating occurs promiscuously with females and males engaging in multiple pair copulations (Hanlon,1998). Since each female is mating with multiple males, there is strong intra-sexual competition both in terms of access to the female for mating, and internal sperm competition post-mating. Two distinct and divergent mating strategies have been selected for and seen in the males to tackle intrasexual competition; the consort strategy and the sneaker strategy. Consorts (Figure 3) compete to mate parallel to the female transferring large quantities of sperm to the female’s oviduct, while Sneakers, as their name suggest, sneak past the consorts and deliver their smaller, but longer-lived spermatophore to secondary receptacles in the female’s buccal mass (Figure 4; Iwata,2011; Hanlon,2006). Which strategy then; quantity or quality would translate to bigger gonads? The answer actually varies across species of Loliginid squid (Chen, 2022), and it all likely comes down to Cryptic Female Choice (CFC).
Photo by Peter Brueggeman, source : http://www.peterbrueggeman.com/photos/img/2011dec5-60.jpg
Photo by Peter Brueggeman, source : http://www.peterbrueggeman.com/photos/img/2011dec5-52.jpg
Videos of mating Doryteuthis squid shoals on YouTube will often show one female being swarmed by a number of different males at any one time. It seems like the females have no say in choosing their mates, but this is simply not true. In Loliginid squid, females exercise post-copulatory mate selection by cryptically ‘choosing’ which male’s sperm to fertilize her eggs with (Sato, 2017). Females hedge their bets between the Consort and Sneaker strategies (as well as between different mates within each strategy) in hopes of maximizing their own fitness (Sato, 2017). Going out on a limb, I would suspect that in most species, CFC is directed strongly towards the consort strategy, as success in this strategy is more body condition dependent, as bigger (healthier) consorts win access to the oviduct. In turn consort males, especially smaller consorts, would have a relatively larger testis to produce more gametes to increase their odds against getting ‘weeded out’ by the female’s CFC. Females would likely benefit from fertilizing a small fraction of eggs with sneaker sperm to ensure some minimum fitness through this strategy in their offspring if the consort fertilized eggs still turn out to be low condition males. The more heavily CFC prefers consort male sperm however(generationally), the stronger the selective pressure on sneakers to produce higher quality sperm to hold on to their fraction of fitness, and the larger the gonads probably would be to accomplish the task.
Hence higher CFC pressure between consorts and sneakers likely results in larger testis in the sneakers, while higher CFC pressure within Consorts would likely result in bigger testis in the consorts.
When thinking about sexual competition, there’ s often a bias to think of the much more visible male vs male competition over female access and fertilization. Cryptic Female Choice opens up a whole new dimension of inter-sexual arms race, revealing the game for securing fitness all the more elaborate. Its astounding to think that something as unapparent as CFC could have such a major impact on male squid anatomical proportions.
References
Hanlon. Mating Systems and Sexual Selection in the Squid Loligo: How might commercial fishing on spawning squid affect them? CalCOFI, Rep., Vol. 39.(1998)
Iwata Yoko , Shaw Paul , Fujiwara Eiji ,Shiba Kogiku & Kakiuchi, Yasutaka & Hirohashi, Noritaka. Why small males have big sperm: Dimorphic squid sperm linked to alternative mating behaviours. BMC evolutionary biology.(2011) 11. 236. 10.1186/1471-2148-11-236.
Pang Y. Chen, CS. Kawamura, T. et al. Environmental influence on life-history traits in male squid Uroteuthis edulis with alternative reproductive tactics. Mar Biol 169, 33 (2022). https://doi.org/10.1007/s00227-022-04017-y
Hanlon, R. T., and J. B. Messenger. Cephalopod Behaviour. Cambridge University Press, Cambridge, England.(1996)
Noriyosi Sato, Masa-aki Yoshida, Takashi Kasugai. 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. Vol71. no.1. pg 112-114. (2017)
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