title: Sperm from sneaker male squids exhibit chemotactic swarming to CO₂.
abstract: 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.
authors.affiliation: Oki Marine Biological Station, Education and Research Center for Biological Resources, Shimane University, 194 Kamo, Okinoshima-cho, Oki, Shimane 685-0024, Japan. hiro@life.shimane-u.ac.jp
authors.forename: Noritaka
authors.initials: N
authors.lastname: Hirohashi
authors.forename: Luis
authors.initials: L
authors.lastname: Alvarez
authors.forename: Kogiku
authors.initials: K
authors.lastname: Shiba
authors.forename: Eiji
authors.initials: E
authors.lastname: Fujiwara
authors.forename: Yoko
authors.initials: Y
authors.lastname: Iwata
authors.forename: Tatsuma
authors.initials: T
authors.lastname: Mohri
authors.forename: Kazuo
authors.initials: K
authors.lastname: Inaba
authors.forename: Kazuyoshi
authors.initials: K
authors.lastname: Chiba
authors.forename: Hiroe
authors.initials: H
authors.lastname: Ochi
authors.forename: Claudiu T
authors.initials: CT
authors.lastname: Supuran
authors.forename: Nico
authors.initials: N
authors.lastname: Kotzur
authors.forename: Yasutaka
authors.initials: Y
authors.lastname: Kakiuchi
authors.forename: U Benjamin
authors.initials: UB
authors.lastname: Kaupp
authors.forename: Shoji A
authors.initials: SA
authors.lastname: Baba
mesh_terms: D000818:Animals; D005075:Biological Evolution; D002245:Carbon Dioxide / Q000378:metabolism*; D002256:Carbonic Anhydrases / Q000378:metabolism; D002633:Chemotaxis; D049832:Decapodiformes / Q000201:enzymology / Q000502:physiology*; D008297:Male; D012098:Reproduction; D013094:Spermatozoa / Q000502:physiology
chemical_list: D002245:Carbon Dioxide; D002256:Carbonic Anhydrases