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ABSTRACT Hybridisation is a common feature of evolutionary radiations, but its genomic consequences vary depending on when it occurs. Since reproductive isolation takes time to accumulate, hybridisation can occur at multiple points during divergence. Previous studies suggested that the taxonomic diversity in evolutionary radiations can help infer the timing of past gene flow events. Here, we assess the power of these approaches for revealing when gene flow occurred between two monkeyflower taxa (Mimulus aurantiacus) endemic to the Channel Islands of California. Coalescent simulations reveal that conventional four‐taxon tests may not be capable of fully distinguishing between recent and ancient introgression, but genome‐wide patterns of phylogenetic discordance vary predictably with different histories of hybridisation. Using whole‐genome sequencing and phylogenetic tests for introgression across theM. aurantiacusradiation, we identify signals of both ancient and recent hybridisation that occurred between the island taxa and their ancestors. In addition, we find widespread selection against introgressed ancestry, consistent with polygenic barriers to gene flow. However, we also identify localised signals across the genome that may indicate adaptive introgression. This study highlights the power and challenges of trying to disentangle complex histories of hybridisation. More broadly, our results illustrate the multiple roles that gene flow can play in evolutionary radiations: hybridisation can expose genetic incompatibilities that contribute to reproductive isolation while also likely facilitating adaptation by transferring beneficial alleles between taxa. These findings underscore the dynamic interplay between the timing of hybridisation and natural selection in shaping evolutionary trajectories within radiations.
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Phylogenomics of a genus of "Great Speciators" reveals rampant incomplete lineage sorting, gene flow, and mitochondrial capture in island systems
The flora and fauna of island systems, especially those in the Indo-Pacific, are renowned for their high diversification rates and outsized contribution to the development of evolutionary theories. The total diversity of geographic radiations of many Indo-Pacific fauna is often incompletely sampled in phylogenetic studies due to the difficulty in obtaining single island endemic forms across the Pacific and the relatively poor performance of degraded DNA when using museum specimens for inference of evolutionary relationships. New methods for production and analysis of genome-wide datasets sourced from degraded DNA are facilitating insights into the complex evolutionary histories of these influential island faunas. Here, we leverage whole genome resequencing (20X average coverage) and extensive sampling of all taxonomic diversity within Todiramphus kingfishers, a rapid radiation of largely island endemic Great Speciators. We find that whole genome datasets do not outright resolve the evolutionary relationships of this clade: four types of molecular markers (UCEs, BUSCOs, SNPs, and mtDNA) and tree building methods did not find a single well-supported and concordant species-level topology. We then uncover evidence of widespread incomplete lineage sorting and both ancient and contemporary gene flow and demonstrate how these factors contribute to conflicting evolutionary histories. Our complete taxonomic sampling allowed us to further identify a novel case of mitochondrial capture between two allopatric species, suggesting a potential historical (but since lost) hybrid zone as islands were successively colonized. Taken together, these results highlight how increased genomic and taxon sampling can reveal complex evolutionary patterns in rapid island radiations.
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- Award ID(s):
- 2112467
- PAR ID:
- 10537990
- Publisher / Repository:
- bioRxiv
- Date Published:
- Format(s):
- Medium: X
- Institution:
- bioRxiv
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript
- Posted Content:
- https://doi.org/10.1101/2024.08.28.610082
