Sperm from Sneaker Male Squids Exhibit Chemotactic Swarming to CO2

SummaryBehavioral 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 [1]. Despite this presumed advantage for reproductive success [2 and 3], 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 [ 4]. 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 Ca2+-dependent turning behavior, resulting in chemotactic swarming. These results illuminate the bifurcating evolution of sperm underlying the distinct fertilization strategies of this species.

Graphical AbstractFigure optionsDownload high-quality image (175 K)Download as PowerPoint slideHighlights
► Small, sneaky squid males produce spermatozoa that swarm to CO2
► Sneaker, but not consort, sperm acidify their intracellular pH due to extracellular acidification by carbonic anhydrase
► Recovery from intracellular acidosis evokes Ca2+-dependent chemotactic swarming
► Swarming by sneaker sperm might be an evolutionary adaptation to mating tactics