Next-generation phylogeography reveals unanticipated population history and climate and human impacts on the endangered floodplain bitterling (Acheilognathus longipinnis)

Abstract

Abstract Background Floodplains harbor highly biodiverse ecosystems, which have been strongly affected by both past climate change and by recent human activities, resulting in a high prevalence of many endangered species in these habitats. Understanding the history of floodplain species over a wide range of timescales can contribute to effective conservation planning. We reconstructed the population formation history of the Itasenpara bitterling Acheilognathus longipinnis, an endangered floodplain fish species in Japan, over a broad timescale based on phylogenetic analysis, demographic modeling, and historical demographic analysis using mitogenome and whole-genome sequences. A genome sequence was newly assembled as a reference for the resequencing analysis. This bitterling is distributed in three plains separated by high mountain ranges and exhibits ecological characteristics well adapted to floodplain environments. Results Our analyses revealed an unexpected population branching pattern, gene flow, and timing of the differentiation that occurred within a few hundred thousand years, i.e., long after the mountain uplift that was assumed to be the primary geological cause of the population differentiation. The analyses also showed that all local populations experienced a severe decline during the last glacial and post-glacial periods. Conclusions Our results suggest that the floodplain bitterling was able to disperse through unknown routes after mountain uplift and that its populations were strongly influenced by climatic and geographic changes in glacial–interglacial cycles and subsequent human activities, probably related to its floodplain-dependent ecology. The genomic data highlight the unanticipated distribution process of this species and the magnitude of the impact of human activities, with important implications for its conservation.

Keywords

• Next-generation phylogeography
• Floodplain
• Historical demography
• Freshwater fish
• Endangered species
• Whole-genome resequencing