Sneaker Male Squid Produce Long-lived Spermatozoa by Modulating Their Energy Metabolism

Abstract

Spermatozoa released by males should remain viable until fertilization. Hence, sperm longevity is governed by intrinsic and environmental factors in accordance with the male mating strategy. However, whether intraspecific variation of insemination modes can impact sperm longevity remains to be elucidated. In the squid Heterololigo bleekeri, male dimorphism (consort and sneaker) is linked to two discontinuous insemination modes that differ in place and time. Notably, only sneaker male spermatozoa inseminated long before egg spawning can be stored in the seminal receptacle. We found that sneaker spermatozoa exhibited greater persistence in fertilization competence and flagellar motility than consort ones because of a larger amount of flagellar glycogen. Sneaker spermatozoa also showed higher capacities in glucose uptake and lactate efflux. Lactic acidosis was considered to stabilize CO 2 -triggered self-clustering of sneaker spermatozoa, thus establishing hypoxia-induced metabolic changes and sperm survival. These results, together with comparative omics analyses, suggest that postcopulatory reproductive contexts define sperm longevity by modulating the inherent energy levels and metabolic pathways.Sperm traits can evolve through postcopulatory contexts involving sperm competition, cryptic female choice, and insemination/fertilization environments. As consequences of sperm competition (1, 2) and cryptic female choice (3, 4), male individuals of certain species have evolved to produce giant spermatozoa to achieve better fertilization success. Besides morphological traits, the evolutionary forces driven by postcopulatory sexual selection should also favor more effective sperm motility and hence influence their morphological and energetic traits (5), thus facilitating fertilization in polyandrous mating systems. Sperm competition theory predicts that an increased risk of sperm competition (sometimes referred to as female promiscuity) should result in selection for increased sperm swimming velocity. A growing body of evidence has supported this prediction. Thus, a positive relationship between sperm swimming speed and sperm competitiveness was seen not only in external fertilizers such as fish (6 -8) but also in internal fertilizers such as birds (9, 10) and mammals (11). Commonly, polyandrous insemination can occur simultaneously (external fertilization) or sequentially (internal fertilization) toward the same set of eggs. However, in species that employ internal fertilization, female individuals often store spermatozoa in their reproductive tract and use them during multiple ovulation cycles (12-14). Thus, it is possible that spermatozoa with greater longevity might have greater reproductive fitness than those with increased velocity. This implicates that spermatozoa should be able to modulate their energy expenditure adequately depending on the postmating contexts.The coastal squid Heterololigo bleekeri exhibits alternative male mating tactics in which complex polyandrous inseminations occur at different places and...

Dimorphic ejaculates and sperm release strategies associated with alternative mating behaviors in the squid

“…In sneakers, slow sperm release may guarantee longer sperm provision, as there may exist an extensive interval between mating and egg release. In the squid Heterololigo bleekeri , longer sperm of sneakers (Iwata et al, ) have prolonged viability when compared to that of consorts (Hirohashi, Tamura‐Nakano, Nakaya, Iida, & Iwata, ). Although we have not investigated how size differences relate to sperm quality traits, sneakers of D. plei also produce longer sperm than consorts (Apostólico & Marian, ).…”

“…In sneakers, slow sperm release may guarantee longer sperm provision, as there may exist an extensive interval between mating and egg release. In the squid Heterololigo bleekeri, longer sperm of sneakers (Iwata et al, 2011) have prolonged viability when compared to that of consorts (Hirohashi, Tamura-Nakano, Nakaya, Iida, & Iwata, 2016).…”

Tactical Tentacles: New Insights on the Processes of Sexual Selection Among the Cephalopoda

“…A multitude of factors can affect sperm competition in animal mating systems. Several of these include: The numbers of males contributing sperm to a female (Parker, 1990), the relative contributions of sperm provided by each male (Parker, 1990), removal of previous males' sperm by subsequent male partners (Birkhead and Hunter, 1990), preferential locations for sperm placement (Naud et al, 2005), differential sperm motility (Birkhead et al, 1999), cryptic female choice (CFC) of sperm (Eberhard, 1996), and differential longevity of sperm and/or stratification of sperm within sperm storage receptacles that can lead to differences in fertilisation success based on the order of copulation by competing males (Birkhead and Hunter, 1990; Naud and Havenhand, 2006; Squires et al, 2015; Hirohashi et al, 2016). The current understanding of how sperm competition might impact cephalopod mating systems is still in its infancy.…”

A coordinated sequence of distinct flagellar waveforms enables a sharp flagellar turn mediated by squid sperm pH-taxis

“…During sea urchin fertilization, sperm chemotaxis can operate once in their life and only at the vicinity of the egg surface 17 , implying the working time to be less than 1 min. By contrast, squid spermatozoa continue clustering for hours after the release from the spermatophore 47 . Thus, the pH sensing system in squid spermatozoa should be persistently sustainable.…”