Origin of scarlet gynogenetic triploid Carassius fish: Implications for conservation of the sexual–gynogenetic complex

Abstract

Conservation of sperm-dependent asexual (gynogenetic) species is challenging due to their complicated ecological dynamics, which requires the stable coexistence with their sperm-providing sexual relatives, who often share similar niches. A symbolic but vulnerable gynogenetic animal is the scarlet Carassius fish, or Hibuna, which is mainly found in Lake Harutori on Hokkaido, Japan. Although Hibuna in Lake Harutori has been protected as a symbol of the Natural Monument of Japan, it has recently suffered population decline. To establish an effective conservation strategy for Hibuna, we investigated its origin, reproductive mode, and genetic diversity, with reference to the surrounding wild populations, using nuclear microsatellites and mitochondrial gene sequences. Our genetic analyses revealed that the main ploidy of Hibuna was triploid or tetraploid, and it reproduces gynogenetically. However, no co-existing sexual diploid Carassius was detected among our samples, suggesting that the sexual diploids and the gynogenetic population including Hibuna would be at risk of co-extirpation. In addition, Hibuna showed high genetic/clonal diversity and most Hibuna had nonindigenous mitochondrial haplotypes that are mostly identical to those reported from goldfish. These results indicate that Hibuna most probably originated from hybridization between indigenous gynogenetic triploids and goldfish introduced about 100 years ago, involving rare sexual reproduction. This spontaneous long-term field experiment exemplifies the recently documented diversification process of gynogenetic Carassius via complex interploidy gene flow. Although the priority to be placed on the conservation of Hibuna is controversial, the maintenance of gynogenetic Carassius, including Hibuna, requires strategic conservation of sexual populations.