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A strategic sampling design revealed the local genetic structure of cold-water fluvial sculpin: a focus on groundwater-dependent water temperature heterogeneity

Abstract

A key piece of information for ecosystem management is the relationship between the environment and population genetic structure. However, it is difficult to clearly quantify the effects of environmental factors on genetic differentiation because of spatial autocorrelation and analytical problems. In this study, we focused on stream ecosystems and the environmental heterogeneity caused by groundwater and constructed a sampling design in which geographic distance and environmental differences are not correlated. Using multiplexed ISSR genotyping by sequencing (MIG-seq) method, a fine-scale population genetics study was conducted in fluvial sculpin Cottus nozawae, for which summer water temperature is the determinant factor in distribution and survival. There was a clear genetic structure in the watershed. Although a significant isolation-by-distance pattern was detected in the watershed, there was no association between genetic differentiation and water temperature. Instead, asymmetric gene flow from relatively low-temperature streams to high-temperature streams was detected, indicating the importance of low-temperature streams and continuous habitats. The groundwater-focused sampling strategy yielded insightful results for conservation.

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Fig. 1: Sampling localities and population structure.
Fig. 2: Mantel correlograms showing spatial autocorrelation of water temperature and genetic data.
Fig. 3: Relationship of genetic differentiation with water temperature and geographic distance.
Fig. 4: Variation in the mean net immigration rate with maximum water temperature.

Data availability

Raw MIG-seq reads were deposited in the DDBJ Sequence Read Archive under accession number DRA011249. The other data are available on Figshare (https://doi.org/10.6084/m9.figshare.13383245).

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Acknowledgements

We are grateful to Jorge García Molinos for support with the data preparation. We thank the staff of the University of Tokyo Hokkaido Forest for their cooperation in selecting study sites. We also thank Suzuki K., Hotta W., Nishio D., Motosugi N., Kawai H., and Zakoh K. of Hokkaido University for their help in conducting the field sampling and laboratory work. We appreciate anonymous reviewers for their valuable comments to the earlier versions of the manuscript. This study is partly supported by the research fund for the Ishikari and Tokachi Rivers provided by the Ministry of Land, Infrastructure, Transport, and Tourism of Japan.

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S.N. and F.N. conceived and designed the study. S.N. and N.I. performed the field work. S.N. and A.M. performed the laboratory work. S.N., M.S., and S.K.H. analyzed the genetic data. S.N. wrote the manuscript, and M.S., S.K.H., N.I., A.M., Y.S., and N.F. edited and revised the manuscript.

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Correspondence to Souta Nakajima.

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Nakajima, S., Sueyoshi, M., Hirota, S.K. et al. A strategic sampling design revealed the local genetic structure of cold-water fluvial sculpin: a focus on groundwater-dependent water temperature heterogeneity. Heredity 127, 413–422 (2021). https://doi.org/10.1038/s41437-021-00468-z

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