The Pacific seaweed pipefish Syngnathus schlegeli exhibits exceptionally high levels of polygynandry among fishes with paternal egg care.

Syngnathid fishes (family Syngnathidae), characterised by male pregnancy via a brood pouch, provide an exceptional model system for studying the relationship between mating systems and sexual selection, as they display extraordinary diversity in both mating systems and sex roles within a single family. A previous study reported that the population of Pacific seaweed pipefish Syngnathus schlegeli around Zhaitang Island in China has a polygamous mating system but did not investigate whether females also mate with multiple partners. In this study, we used parentage analyses with eight microsatellite markers to investigate the genetic mating system of a northern population of S. schlegeli in Mutsu Bay, Japan. All pregnant males carried full broods of 942-1729 embryos, and paternity was exclusively assigned to the brooding male. Males mated with an average of five females (range 3-9), and eggs from different females were spatially segregated within each brood pouch. The occurrence of shared maternity across broods from different males indicated that females also performed multiple matings; however, females had a lower number of mates than males. These results clearly demonstrated that the Mutsu Bay population of S. schlegeli has a polygynandrous mating system. Notably, the maximum of nine mates per male represents the highest number of multiple matings reported for syngnathid fishes and possibly for fishes with paternal egg care. We suggest that the unusually high number of mates per male may be linked to the sexual size dimorphism in this population, where males are larger than females, which is a rare pattern among syngnathids. The comparison between the Zhaitang Island population and the Mutsu Bay population of S. schlegeli revealed clear geographic variations in body size, brood size and the number of mates per male. These patterns in S. schlegeli are similar to intraspecific latitudinal trends reported in some Syngnathus species, in which higher-latitude populations tend to have greater body size, greater brood size and more mates per male. Further studies across a broader geographic range are needed to verify whether S. schlegeli exhibits latitudinal variation in mating systems.