Behavioral traits of sperm are adapted to the reproductive strategy that each species employs. In polyandrous species, spermatozoa often form motile clusters, which might be advantageous for competing with sperm from other males. Despite this presumed advantage for reproductive success, little is known about how sperm form such functional assemblies. Previously, we reported that males of the coastal squid Loligo bleekeri produce two morphologically different euspermatozoa that are linked to distinctly different mating behaviors. Consort and sneaker males use two distinct insemination sites, one inside and one outside the female's body, respectively. Here, we show that sperm release a self-attracting molecule that causes only sneaker sperm to swarm. We identified CO2 as the sperm chemoattractant and membrane-bound flagellar carbonic anhydrase as its sensor. Downstream signaling results from the generation of extracellular H(+), intracellular acidosis, and recovery from acidosis. These signaling events elicit Ca(2+)-dependent turning behavior, resulting in chemotactic swarming. These results illuminate the bifurcating evolution of sperm underlying the distinct fertilization strategies of this species.

In yeast, plant, and mammalian somatic cells, short poly(A) tails on mRNAs are subject to uridylation, which mediates mRNA decay. Although mRNA uridylation has never been reported in animal oocytes, maternal mRNAs with short poly(A) tails are believed to be translationally repressed. In this study, we found that 96% of cyclin B mRNAs with short poly(A) tails were uridylated in starfish oocytes. Hormonal stimulation induced poly(A) elongation of cyclin B mRNA, and 62% of long adenine repeats did not contain uridine residues. To determine whether uridylated short poly(A) tails destabilize cyclin B mRNA, we developed a method for producing RNAs with the strict 3 ′ terminal sequences of cyclin B, with or without oligo(U) tails. When we injected these synthetic RNAs into starfish oocytes prior to hormonal stimulation, we found that uridylated RNAs were as stable as nonuridylated RNAs. Following hormonal stimulation, the 3 ′ termini of short poly(A) tails of synthesized RNAs containing oligo(U) tails were trimmed, and their poly(A) tails were subsequently elongated. These results indicate that uridylation of short poly(A) tails in cyclin B mRNA of starfish oocytes does not mediate mRNA decay; instead, hormonal stimulation induces partial degradation of uridylated short poly(A) tails in the 3 ′ -5 ′ direction, followed by poly(A) elongation. Oligo(U) tails may be involved in translational inactivation of mRNAs.

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Meiotic progression requires the translation of maternal mRNAs in a strict temporal order. In isolated animal oocytes, translation of maternal mRNAs containing a cytoplasmic polyadenylation element (CPE), such as cyclin B, is activated by in vitro stimulation of meiotic resumption which induces phosphorylation of CPEB (CPE-binding protein) and elongation of their polyadenosine (poly(A)) tails; whether or not this model can be applied in vivo to oocytes arrested at metaphase of meiosis I in ovaries is unknown. In this study, we found that active CDK1 (cyclin-dependent kinase 1) phosphorylated CPEB in ovarian oocytes arrested at metphase I in the starfish body cavity, but phosphorylation of CPEB was not sufficient for elongation of cyclin B poly(A) tails. Immediately after spawning, however, mRNA was polyadenylated, suggesting that an increase in intracellular pH (pHi ) upon spawning triggers the elongation of poly(A) tails. Using a cell-free system made from maturing oocytes at metaphase I, we demonstrated that polyadenylation was indeed suppressed at pH below 7.0. These results suggest that a pH-sensitive process, functioning after CPEB phosphorylation, is blocked under physiologically low pHi (<7.0) in metaphase-I-arrested oocytes. The increase in pHi (>7.0) that occurs after spawning triggers polyadenylation of cyclin B mRNA and progression into meiosis II.