Why small males have big sperm: dimorphic squid sperm linked to alternative mating behaviours

Abstract

BackgroundSperm cells are the target of strong sexual selection that may drive changes in sperm structure and function to maximize fertilisation success. Sperm evolution is regarded to be one of the major consequences of sperm competition in polyandrous species, however it can also be driven by adaptation to the environmental conditions at the site of fertilization. Strong stabilizing selection limits intra-specific variation, and therefore polymorphism, among fertile sperm (eusperm). Here we analyzed reproductive morphology differences among males employing characteristic alternative mating behaviours, and so potentially different conditions of sperm competition and fertilization environment, in the squid Loligo bleekeri.ResultsLarge consort males transfer smaller (average total length = 73 μm) sperm to a female's internal sperm storage location, inside the oviduct; whereas small sneaker males transfer larger (99 μm) sperm to an external location around the seminal receptacle near the mouth. No significant difference in swimming speed was observed between consort and sneaker sperm. Furthermore, sperm precedence in the seminal receptacle was not biased toward longer sperm, suggesting no evidence for large sperm being favoured in competition for space in the sperm storage organ among sneaker males.ConclusionsHere we report the first case, in the squid Loligo bleekeri, where distinctly dimorphic eusperm are produced by different sized males that employ alternative mating behaviours. Our results found no evidence that the distinct sperm dimorphism was driven by between- and within-tactic sperm competition. We propose that presence of alternative fertilization environments with distinct characteristics (i.e. internal or external), whether or not in combination with the effects of sperm competition, can drive the disruptive evolution of sperm size.

Nocturnal mating behaviour and dynamic male investment of copulation time in the southern blue-ringed octopus, Hapalochlaena maculosa (Cephalopoda: Octopodidae)

“…Specifically, these results support findings by Cigliano (1995) and Wada et al (2010) in that some male cephalopods appear to strategically regulate their copulation time based on the mating history of the female, presumably to maximise their reproductive output by balancing both their chance of paternity and their ability to successfully copulate with other females. Sperm competition appears prevalent among cephalopod mating systems (Cigliano, 1995;Hanlon et al, 1999;Naud et al, 2004;Shaw & Sauer, 2004;Wada et al, 2005b;Wada et al, 2006;Buresch et al, 2009;Wada et al, 2010;Iwata et al, 2011;Sato et al, 2013). Future studies using molecular markers might identify correlations between paternity and behavioural patterns including copulation duration and chronology.…”

Respiratory CO2 Mediates Sperm Chemotaxis in Squids

“…Although a factor that infl uences the male-type decision remains to be identifi ed, this system offers extremely a unique situation where internal and external fertilization coexist within a single spawning episode. Previously, we found that sneaker sperm are ~50 % longer than consort sperm (Iwata et al 2011 ). Although no such clear within-species dimorphic eusperm had been reported previously, there are many examples of sperm size differences among closely related species, which have largely been explained as the consequences of sperm competition (Gage 1994 ;Briskie and Montgomerie 1992 ;Gomendio and Roldan 1991 ).…”

“…Despite extended arguments on the evolutionary adaptation of sperm cooperation for reproductive success (Immler 2008 ;Foster and Pizzari 2010 ), little is known about how sperm form functional conjugates (Moore et al 2002 ). Previously, we found that each male of the coastal squid Loligo bleekeri produces one of two types of morphologically distinct euspermatozoa , the two types being linked to distinctly different male mating behaviors (Iwata et al 2011 ). Consort males produce spermatozoa with short fl agella and transfer sperm capsules (spermatophores ) to internal locations of the females, inside the oviduct, whereas sneaker males produce long-fl agellum sperm and transfer spermatophores to the outer body wall of the same females ( Fig.…”

“…Unexpectedly, empirical data supported no evidence that larger sperm are favored in sperm competition in this species regarding the swimming velocity and sperm precedence at the storage site (in the seminal receptacle). Alternatively, different fertilization environments might be a prominent factor that could drive the evolution of sperm size (Iwata et al 2011 ).…”

“…Consort males produce spermatozoa with short fl agella and transfer sperm capsules (spermatophores ) to internal locations of the females, inside the oviduct, whereas sneaker males produce long-fl agellum sperm and transfer spermatophores to the outer body wall of the same females ( Fig. 2.1 , Iwata et al 2011 ). The evolutionary consequences by which such phenotypic dimorphism arose remain elusive; however, each In L. bleekeri , male individuals conduct one of two alternative reproductive tactics associated with body size.…”