Even short‐distance dispersal over a barrier can affect genetic differentiation in Gyraulus, an island freshwater snail

• Published in: Freshwater biology 2022-11, Vol.67 (11), p.1971-1983
• Main Authors: Saito, Takumi, Sasaki, Tetsuro, Tsunamoto, Yoshihiro, Uchida, Shota, Satake, Kiyoshi, Suyama, Yoshihisa, Chiba, Satoshi
• Format: Article
• Language: English
• Subjects: Bayesian analysis; Biodiversity; Catchment area; Computation; Deoxyribonucleic acid; Differentiation; Dispersal; Dispersion; Distance; Divergence; DNA; Dynamics; Evolutionary genetics; Freshwater; freshwater gastropod; Freshwater molluscs; Gene flow; Genetic analysis; Genetic diversity; Genetic structure; Genomes; Geography; Gyraulus; Inland water environment; Landscape; Landscape ecology; long‐distance dispersal; MIG‐seq; Mitochondrial DNA; Molecular structure; Nucleotides; Oceanic islands; Phylogenetics; Phylogeny; Planorbidae; Pleistocene; Pliocene; Population genetics; Probability theory; Snails; world heritage site
• ISSN: 0046-5070; 1365-2427
• DOI: 10.1111/fwb.13990

Dispersal is a fundamental mechanism for maintaining biodiversity, and long‐distance dispersal (LDD) has attracted the interest of many researchers owing to its unusual characteristics. Conventionally, LDD has been defined based on absolute and proportional distances; however, it has recently been redefined based on geographic and genetic limits. Based on this redefinition, short‐distance dispersal can have the same characteristics as LDD, depending upon the dispersal dynamics of an organism. However, the effects of LDD at a local scale on the genetic structure and diversification of organisms are poorly understood, since many studies have focused on definitive LDD, such as oversea dispersal. We focused on the freshwater snail Gyraulus sp. on an oceanic island, Chichijima Island, attempting to clarify the dynamics and effects of LDD on its genetic structure. We conducted molecular phylogenetic analyses, including divergence‐time estimation, using mitochondrial DNA and nuclear DNA markers to reveal the origin of the snail. In addition, we clarified the genetic structure, gene flow, and evolutionary history of snails on the island using mitochondrial DNA and genome‐wide single‐nucleotide polymorphisms. Finally, we followed a landscape ecology approach to identify barriers to dispersal. Our phylogenies suggested that the snail has a single origin. Based on our divergence–time estimation, colonisation was estimated to have occurred around the late Pliocene to early Pleistocene. Our population genetic analyses documented genetic differentiation even within this small oceanic island. Based on the divergence time estimation and approximate Bayesian computation using single‐nucleotide polymorphisms, the differentiation was estimated to have begun around the late Pleistocene. Little gene flow occurred between the geographically structured snail genetic groups. Landscape analysis suggested that catchment boundaries were a major barrier to dispersal. Considering the geography of the island, these results suggested that low‐frequency dispersal over barriers is an important factor in genetic differentiation within the island. Furthermore, dispersal over barrier may be considered LDD, even though the dispersal distance is only several kilometres. Genetic evidence also suggested that resistance to gene flow over the barrier, rather than distance, is more important in determining whether dispersal should be considered LDD. This suggests that a definition of LDD that depen