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

Noritaka Hirohashi,Miwa Tamura-Nakano,Fumio Nakaya,Tomohiro Iida,Yoko Iwata

doi:10.1074/jbc.m116.737494

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 CO2-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.

Highlights

Sperm traits can evolve through postcopulatory contexts involving sperm competition, cryptic female choice, and insemination/fertilization environments
The data clearly showed that, higher fertilization rates were obtained in both types of sperm shortly after recovery from the spermatangium, fertilization competence was lost within 20 min in consort spermatozoa, whereas it remained unchanged for 45 min in sneaker spermatozoa (Fig. 2A)
We further examined sneaker spermatozoa recovered from the seminal receptacle, the sperm storage organ of the female

Summary

Introduction

Sperm traits can evolve through postcopulatory contexts involving sperm competition, cryptic female choice, and insemination/fertilization environments. Promiscuous copulations by both sneaker and consort males occur just prior to egg spawning so that the durations between sperm insemination and fertilization are short. “sneaker” males copulate with females at much earlier times before egg spawning Thereafter, their spermatozoa inseminated at the buccal membrane of the female migrate to the seminal receptacle and survive for an extended duration such as days or even months [16, 17]. Sneaker spermatozoa are, in general, more costly than consort ones in terms of the total amount of energy required for accomplishing fertilization. In this context, we speculated that sneaker spermatozoa would have expanded their metabolic system, allowing on-demand energy production and storage [12]. We conducted comparative analyses between sneaker and consort male squid in terms of sperm metabolism and related functions such as motility, longevity, and sustainability of fertilizing competence

Methods

Results

Conclusion