Elucidating river history through population genetics of an aquatic organism

Rivers sometimes change their way, caused by geological events. During such river rearrangement, what happened to the inhabitants? We investigated the genetic traces remaining in genomes of the descendants and look for a way to find unidentified geological events.

Above: An upper reach of mountain stream on Honshu Island, Japan.

Honshu Island, the main island of the Japan archipelago, has a mountainous landscape with a complex array of strike-slip and thrust faults. Numerous streams rise from the mountain ranges called the Central Divide of Japan, where two major watersheds are divided (The Sea of Japan and the Pacific watersheds). However, the drainage divide is not always apparent, and headwaters of different drainages are close to each other in some locations. As a regional angler, I was wondering if these rivers were connected or disconnected easily by heavy rainfalls, general climate change or geomorphological movement. If so, what happened in aquatic organisms, particularly to their genetic structures and distributions, when their habitats were drastically changed? Accordingly, thinking that stream capture, in which an upper stream of a river is captured by and displaced to another adjacent river, should have a prominent impact on the gene flow of stream fishes, then the history of the landscape should have synchronized the ecology of aquatic organisms. Thus, population genetics should be a good candidate as a witness of the geological events.

White-spotted charr is a stenothermal cold-water adopted salmonid distribute in North-eastern Pacific, including the Japan archipelago. This species is generally landlocked in the upper streams in Honshu Island, the edge of their distribution. These characteristics would meet requirements bearing witness to geological events (unless there had been human mediated translocation). First, we investigated the genetic structure of white-spotted charr from three major watersheds, the Sea of Japan, the Pacific and Lake Biwa. Samples were collected from the upper reaches close to the divides to avoid the bias of artificial stockings. As a result, fish from three major watersheds were clearly classified into three distinctive genetic structures (Fig. 2).

Editors’ choice article: (Free to read online for two years.)
Masuda, T., Shimono, Y., Kishi, D., & Koizumi, I. (2023). Systematic headwater sampling of white-spotted charr reveals stream capture events across dynamic topography. Journal of Biogeography, 50, 453– 466. https://doi.org/10.1111/jbi.14553

However, we found several exceptions in which genetic structure of charr was inconsistent with the current watershed group. One such exception was seen at a site known to have experienced stream capture (Fig. 3). Although site J1 belongs to the Sea of Japan watershed now, fish from the site were perfectly classified to the Lake Biwa genetic cluster. This result is completely consistent with the history of the river capture, in which site J1 used to be upstream of site B1, and subsequently, the catchment including J1 was captured by the river flowing north to the Sea of Japan, resulting in isolation from B1. In accordance with the geological history, the genetic structure of J1 charr was completely assigned to the Lake Biwa genetic group almost without contamination with genes from the Sea of Japan group. Thus, the population at J1 is a subdivision of the Lake Biwa genetic group, and designated as an ‘exclave case’. It would have been impossible for downstream fish (the Sea of Japan group) to move up into J1 territory because of some intervening gorges and steep waterfalls. The exclave case would be a typical consequence of river capture events. We found another example of an exclave in which the Pacific and Lake Biwa genetic group were related, indicating the unidentified broad area drainage rearrangement.

Typical individuals of white-spotted charr from the Sea of Japan (upper), the Pacific (middle) and Lake Biwa (bottom).

We also observed other genetic and regional inconsistencies that produced genetic admixture in some locations near the divides. This pattern could be a trace of the transient river connections by natural phenomena, although some of such cases might be attributed to human mediated translocation.

(a) Population genetic structure of white-spotted charr from the sample sites. (b) Genetic structure of some populations from the three major watersheds.(c) An example of a population illustrating the “exclave” pattern.

Thus, we proposed the possibility to discover the geological history of drainage rearrangement from the genetic aspects of aquatic organisms. Verification with other aquatic species including invertebrates would further support the hypotheses. We are investigating the genetic structure of Rhynchocypris oxycephalus and Cottus pollux from the locations with probable stream capture history in addition to sites of the current research.

Written by:
Taro Masuda1, Yoshiko Shimono2, Daisuke Kishi3 and Itsuro Koizumi4
1Laboratory of Marine Biology, Faculty of Agriculture, Setsunan University, 45-1 Nagaotoge-cho, Hirakata, Osaka, 573-0101, Japan
2 Laboratory of Weed Science, Division of Agronomy and Horticultural Science, Graduate School of Agriculture, Kyoto University, Kitashirakawa-Oiwake Cho, Kyoto
3 Gero Branch, Gifu Prefectural Research Institute for Fisheries and Aquatic Environments, 2605-1 Hane, Hagiwara, Gero, Gifu, 509-2592, Japan
4 Faculty of Environmental Earth Science, Hokkaido University, N10W5 Sapporo, Hokkaido 060-0810, Japan

Published by jbiogeography

Contributing to the growth and societal relevance of the discipline of biogeography through dissemination of biogeographical research.

Leave a Reply

%d bloggers like this: