Evidence for sympatric speciation in a Wallacean ancient lake

Abstract

Sympatric speciation has been demonstrated in few empirical case studies, despite intense searches, because of difficulties in testing the criteria for this mode of speciation. Here, we report a possible case of sympatric speciation in ricefishes of the genus Oryzias on Sulawesi, an island of Wallacea. Three species of Oryzias are known to be endemic to Lake Poso, an ancient tectonic lake in central Sulawesi. Phylogenetic analyses using RAD‐seq‐derived single nucleotide polymorphisms (SNPs) revealed that these species are monophyletic. We also found that the three species are morphologically distinguishable and clearly separated by population‐structure analyses based on the SNPs, suggesting that they are reproductively isolated from each other. A mitochondrial DNA chronogram suggested that their speciation events occurred after formation of the tectonic lake, and existence of a historical allopatric phase was not supported by coalescent‐based demographic inference. Demographic inference also suggested introgressive hybridization from an outgroup population. However, differential admixture among the sympatric species was not supported by any statistical tests. These results all concur with criteria necessary to demonstrate sympatric speciation. Ricefishes in this Wallacean lake provide a promising new model system for the study of sympatric speciation.

Mitochondrial introgression by ancient admixture between two distant lacustrine fishes in Sulawesi Island

“…For the O. sarasinorum and O. eversi individuals, genomic data were generated by ddRAD-seq [20] (see [15] for details of library preparations). The library was sequenced with 50-bp single-end reads on an Illumina HiSeq 2500 system (Illumina, San Diego, USA) by Macrogen Japan Corporation (Kyoto, Japan).…”

“…Sequence trimming and mapping to a genome assembly of an O. celebensis individual (Ansai et al, unpublished data) were performed as described in [15].…”

“…However, it is possible that the lake did not just undergo division. Some tectonic lakes and lake systems are known to have undergone repeated fragmentations and fusions, which caused repeated isolations and admixtures of lacustrine organisms [15].…”

“…Oryzias and Adrianichthys, a larger adrianichthyid genus [32], just like O. sarasinorum [34]. Although the exact generation time for these species remains unknown, assuming a generation time of 2 years as in [15], our coalescent-base demographic inference estimated that their divergence was approximately 170,000 (158,000-317,000) years ago. Therefore, we think that †L.…”

“…would have occurred ca. 260,000-322,000 years ago assuming a substitution rate of 2.5%-3.1% per million years [35], which has been used for divergence-time estimation of Sulawesi adrianichthyids [2,11,15]. This discrepancy may indicate that the synonymous substitution rate used in the demographic inference (i.e., 3.5 × 10 −9 per site and generation) was too high.…”