Toward conservation of genetic and phenotypic diversity in Japanese sticklebacks

Abstract

Stickleback fishes have been established as a leading model system for studying the genetic mechanisms that underlie naturally occurring phenotypic diversification. Because of the tremendous diversification achieved by stickleback species in various environments, different geographical populations have unique phenotypes and genotypes, which provide us with unique opportunities for evolutionary genetic research. Among sticklebacks, Japanese species have several unique characteristics that have not been found in other populations. The sympatric marine threespine stickleback species Gasterosteus aculeatus and G. nipponicus (Japan Sea stickleback) are a good system for speciation research. Gasterosteus nipponicus also has several unique characteristics, such as neo-sex chromosomes and courtship behaviors, that differ from those of G. aculeatus. Several freshwater populations derived from G. aculeatus (Hariyo threespine stickleback) inhabit spring-fed ponds and streams in central Honshu and exhibit year-round reproduction, which has never been observed in other stickleback populations. Four species of ninespine stickleback, including Pungitius tymensis and the freshwater, brackish water and Omono types of the P. pungitius-P. sinensis complex, are also excellent model systems for speciation research. Anthropogenic alteration of environments, however, has exposed several Japanese stickleback populations to the risk of extinction and has actually led to extinction of several populations and species. Pungitius kaibarae, which is endemic to East Asia, used to inhabit Kyoto and Hyogo prefectures, but is now extinct. Causes of extinction include depletion of spring water, landfill of habitats, and construction of rivermouth weirs. Here, we review the importance of Japanese sticklebacks as genetic resources, the status of several endangered stickleback populations and species, and the factors putting these populations at risk.

Parallel transcriptome evolution in stream threespine sticklebacks

“…Generally, the different magnitudes of divergence can result from differences in divergence time, gene flow, and/or selection regimes (Berner, Roesti, Hendry, & Salzburger, ; Stuart et al., ). In the Little Campbell River, the marine and stream ecotypes are parapatric, with their hybrid zone existing in the midstream (Hagen, ), whereas the stream habitat in Gifu, Japan, is isolated from the sea, making the gene flow between marine and stream ecotypes unlikely (Kitano & Mori, ; Mori, ). The time of freshwater colonization in British Columbia, Canada, is thought to be postglacial (Bell & Foster, ), whereas that of the Japanese stream population was estimated to be much older, such as 0.37–0.43 million years ago, by an analysis of mitochondrial cytochrome b sequence (Watanabe, Mori, & Nishida, ).…”

Multiple waves of freshwater colonization of the three-spined stickleback in the Japanese Archipelago

“…Sticklebacks favor a cooler climate [11,41], so they would expand the distribution southward during glacial periods and retract northward during interglacial periods [37]. Freshwater populations in central Honshu Island are presently restricted to springs and spring-fed streams in which water temperature is maintained below 20 °C, allowing the sh to avoid heat in summer [24,41]. Habitats of the hariyo stickleback and the Nasu population are on the Paci c slope, out of the current distribution range of marine G. aculeatus.…”

“…For example, non-native populations from FW Kobe [K] and FW Komono [J] were derived from either Aizu or FW Nasu [u] populations. Although non-native populations can provide opportunities to study the process of adaptation to novel habitats on a contemporary timescale [27,28], their spread may lead to hybridization with, or extinction, of native populations [24]. Native freshwater populations are invaluable genetic resources to study the genetic basis of adaptive phenotypic diversi cation generated during the last 200,000 years in the Japanese Archipelago.…”

“…The distribution range of marine G. aculeatus, which overlaps with that of G. nipponicus in the Japanese Archipelago, is hatched in dark blue. The distribution ranges followed those of Higuchi [96], Higuchi et al [29], Kitano and Mori [24] and Yoshigou [97]. The map was created with rnaturalearth ver.…”

“…The Japanese Archipelago was not covered by ice sheets in the Quaternary glaciation, suggesting that several freshwater habitats were accessible by sticklebacks well before 12,000 years ago. A previous mitochondrial DNA phylogenetic analysis estimated the divergence time of freshwater populations in Gifu and Shiga, central Honshu Island, termed 'hariyo stickleback' in Japan [23,24], from the rest of G. aculeatus as 0.37-0.43 million years before present (Ma BP) based on a molecular clock. Additionally, there are several young freshwater populations.…”