Rapid sexual reproduction intensifies blooms of a mixotrophic dinoflagellate

Sexual reproduction is fundamental to the ecology and evolution of eukaryotes, yet its dynamics in microbial eukaryotes are often cryptic. Dinophysis are specialist mixotrophs that must balance prey capture, cell division, and sexual recombination during blooms, but relatively little is known about the occurrence and role of sex in their ecology. Here, mating was investigated in D. acuminata through continuous automated microscopy of cultured cells and throughout two blooms within the Nauset Marsh estuary (Massachusetts, USA). Across these studies, vegetative division and mating were phased on a diel timescale, occurring primarily at night and near dawn, regardless of prey availability. Mating and division were determined to be linked based on sequencing of their phases, correlation of their daily frequencies, and their reestablishment after a 2‐d light block during the culture experiment. Mating was not associated with zygote accumulation or resting stage formation, but rapid cell reproduction via meiosis. It was also the dominant mode of reproduction during blooms, accounting for 71% and 64% of the new cell production recorded in 2015 and 2021, respectively. Because it is dependent on gamete encounters, sexual reproduction is increasingly accessible as blooms develop. This reliance on sexual reproduction is an example of Red Queen dynamics; meiotic recombination enhances genotypic diversity within blooms, enhancing resilience to pathogens, parasites, and other threats that intensify as cell densities increase.