Wowor, D. | bioRxiv Science

bioRxiv2025

Multiple instances of river-lake introgression in the adaptive radiation of sailfin silversides in Wallace's Dreampond

While adaptive radiations significantly contribute to the worlds biodiversity, much is unknown about the genetic and ecological factors underlying these rapid successions of speciation. It has been suggested that hybridisation can facilitate the speciation process by generating genetic diversity on which diversifying selection can act. Sailfin silverside fishes (Telmatherinidae) in the Malili Lakes system in Sulawesi have diversified within the last 2 million years. We assembled and annotated a chromosome-scale reference genome of the riverine sailfin silverside Telmatherina bonti and generated whole genome sequences of all species of Telmatherina in Lake Matano, South Sulawesi, Indonesia, one of the worlds oldest and deepest lakes. We reconstructed the phylogenetic relationships within the adaptive radiation of sailfin silversides and inferred past and ongoing introgression patterns. Genome-wide tests confirmed two monophyletic clades, sharpfins and roundfins. However, within clades, we found mismatches between morphology-based taxonomic assignments and genome-wide genetic relationships. We found signs of both old and ongoing introgression between river-dwelling T. bonti and the lacustrine sharpfin group, as shown in elevated D-statistic, f4-ratio and f-branch statistic. Levels of excess allele sharing between riverine species and the three most common lacustrine species declined with increasing distance from the river-inlet, indicating ongoing introgression at the lake-river interface. This combination of past and ongoing hybridisation in a radiating species flock makes Lake Matano Telmatherina a particularly valuable system to study fundamental mechanisms driving rapid speciation under genomic exchange. The phylogenomic framework elaborated in this study provides the foundation for studies of the processes shaping this charismatic radiation.

evolutionary biology↗

bioRxiv2022

Contribution of hybridization to the evolution of a derived reproductive strategy in ricefishes

Transitions between reproductive strategies are costly and involve major changes in life history, behaviour and morphology. Nevertheless, in Sulawesi ricefishes, pelvic-brooding evolved from transfer-brooding in two distantly related lineages within in the genera Adrianichthys and in Oryzias, respectively. Females of pelvic-brooding species carry their eggs attached to their belly until the fry hatches. Despite their phylogenetic distance, both pelvic-brooding lineages share a set of external morphological traits. A recent study found no direct gene-flow between pelvic-brooding lineages suggesting independent evolution of the derived reproductive strategy. It could, however, also be more complex. Pre-existing variation in an admixed population may enable the re-use of genetic variants when subjected to similar external selection pressure, resulting in similar phenotypes. We thus used a multi-species coalescent (MSC) model and D-statistics to identify gene-tree - species-tree incongruencies, to evaluate the evolution of pelvic-brooding with respect to inter-specific gene-flow not only between pelvic-brooding lineages, but between pelvic-brooding lineages and other Sulawesi ricefish lineages. We found a general network-like evolution in Sulawesi ricefishes and as previously reported, no gene-flow between the pelvic-brooding lineages. Instead, we found hybridization between the ancestor of pelvic-brooding Oryzias and the common ancestor of the four Oryzias species from Lake Poso, home of the pelvic-brooding Adrianichthys lineage. Further, indications of introgression were located within two confidence intervals of quantitative trait loci (QTL) associated with pelvic-brooding in O. eversi. We thus hypothesize that a mix of de novo mutations and (ancient) standing genetic variation shaped the evolution of pelvic-brooding. Significance statementThe evolution of pelvic-brooding in Oryzias eversi (Beloniformes:Adrianichthyidae), was recently described to be independent from another pelvic-brooding ricefish lineage (Adrianichthys) from Sulawesi. We confirmed these results, and detected no gene flow between the two distantly related pelvic-brooding lineages. Instead, we found ancient gene flow from another Orzyias lineage into the pelvic-brooding Oryzias lineage. One of the previously described QTL for pelvic brooding overlaps with a region of high introgression signal. Therefore, we assume that not only de novo mutations contributed to the evolution of pelvic-brooding in Orzyias, but that introduced ancient genetic variation was likely also recruited for the evolution of this derived brooding strategy.

evolutionary biology↗