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Background <p>Biotic diversification in ancient lakes is shaped by complex geological histories and genetic exchange among populations. The Malili Lake system on Sulawesi Island represents a classic natural laboratory for studying freshwater fish evolution and harbors multiple endemic <i>Oryzias</i> species that diversified under repeated hydrological reorganizations. Previous genomic analyses inferred that two sympatric species in Lake Towuti (<i>O. profundicola</i> and <i>O. loxolepis</i>) experienced a single ancient introgression event from a “ghost lineage” derived from <i>O. marmoratus</i> inhabiting another lake. However, recent taxonomic re-evaluation has revealed the presence of an extant <i>O. marmoratus</i> population within Lake Towuti itself. This finding suggests that the putative ghost lineage may in fact represent a living population co-occurring in the lake, calling for a re-examination of the introgression history and speciation mode in Lake Towuti.</p> Results <p>By incorporating newly generated ddRAD-seq data from the true <i>O. marmoratus</i> in Lake Towuti, we reanalyzed phylogenetic relationships and population genetic structure among Malili Lake <i>Oryzias</i>. Previously reported major phylogenetic relationships and inter-lake introgression patterns were largely reproduced. In contrast, TreeMix and <i>f</i><sub><i>4</i></sub>-statistic analyses revealed that introgression signals previously attributed to a “ghost lineage” into <i>O. profundicola</i> and <i>O. loxolepis</i> instead originated from the extant <i>O. marmoratus</i> population coexisting within Lake Towuti. Demographic model comparisons explicitly incorporating within-lake gene flow further supported a scenario in which <i>O. profundicola</i> and <i>O. loxolepis</i> diverged in allopatry, subsequently came into secondary contact within Lake Towuti, and later experienced additional gene flow following secondary contact with <i>O. marmoratus</i> that entered the lake.</p> Conclusion <p>Our results demonstrate that introgression from the <i>O. marmoratus</i> lineage into <i>O. profundicola</i> and <i>O. loxolepis</i> was not a single ancient event, but rather a more sustained process. This finding highlights the critical importance of taxonomic resolution for accurately inferring introgression and divergence history. Comparative studies across other ancient lakes on Sulawesi will be valuable for understanding how the timing and nature of gene flow from third lineages influence patterns of population divergence and the strength of reproductive isolation.</p>

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Revised taxonomy reveals sustained introgression and secondary contact in ancient lake ricefishes

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2026年5月12日

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  • Yuki Yashima,
  • Andy B. Nofrianto,
  • Handung Nuryadi,
  • Ryo Kakioka,
  • Hirozumi Kobayashi,
  • Satoshi Ansai,
  • Ixchel F. Mandagi,
  • Kawilarang W. A. Masengi,
  • Sjamsu A. Lawelle,
  • Atsushi J. Nagano,
  • Junko Kusumi,
  • Kazunori Yamahira

摘要

Background

Biotic diversification in ancient lakes is shaped by complex geological histories and genetic exchange among populations. The Malili Lake system on Sulawesi Island represents a classic natural laboratory for studying freshwater fish evolution and harbors multiple endemic Oryzias species that diversified under repeated hydrological reorganizations. Previous genomic analyses inferred that two sympatric species in Lake Towuti (O. profundicola and O. loxolepis) experienced a single ancient introgression event from a “ghost lineage” derived from O. marmoratus inhabiting another lake. However, recent taxonomic re-evaluation has revealed the presence of an extant O. marmoratus population within Lake Towuti itself. This finding suggests that the putative ghost lineage may in fact represent a living population co-occurring in the lake, calling for a re-examination of the introgression history and speciation mode in Lake Towuti.

Results

By incorporating newly generated ddRAD-seq data from the true O. marmoratus in Lake Towuti, we reanalyzed phylogenetic relationships and population genetic structure among Malili Lake Oryzias. Previously reported major phylogenetic relationships and inter-lake introgression patterns were largely reproduced. In contrast, TreeMix and f4-statistic analyses revealed that introgression signals previously attributed to a “ghost lineage” into O. profundicola and O. loxolepis instead originated from the extant O. marmoratus population coexisting within Lake Towuti. Demographic model comparisons explicitly incorporating within-lake gene flow further supported a scenario in which O. profundicola and O. loxolepis diverged in allopatry, subsequently came into secondary contact within Lake Towuti, and later experienced additional gene flow following secondary contact with O. marmoratus that entered the lake.

Conclusion

Our results demonstrate that introgression from the O. marmoratus lineage into O. profundicola and O. loxolepis was not a single ancient event, but rather a more sustained process. This finding highlights the critical importance of taxonomic resolution for accurately inferring introgression and divergence history. Comparative studies across other ancient lakes on Sulawesi will be valuable for understanding how the timing and nature of gene flow from third lineages influence patterns of population divergence and the strength of reproductive isolation.