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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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Genomic patterns in the dwarf kingfishers of northern Melanesia reveal a mechanistic framework explaining the paradox of the great speciators
Abstract The paradox of the great speciators describes a contradictory biogeographic pattern exhibited by numerous avian lineages in Oceania. Specifically, these lineages display broad geographic distributions across the region, implying strong over-water dispersal capabilities; yet, they also display repeated genetic and phenotypic divergence—even between geographically proximate islands—implying poor inter-island dispersal capabilities. One group originally cited as evidence for this paradox is the dwarf kingfishers of the genus Ceyx. Here, using genomic sequencing and comprehensive geographic sampling of the monophyletic Ceyx radiation from northern Melanesia, we find repeated, deep genetic divergence and no evidence for gene flow between lineages found on geographically proximate islands, providing an exceptionally clear example of the paradox of the great speciators. A dated phylogenetic reconstruction suggests a significant burst of diversification occurred rapidly after reaching northern Melanesia, between 3.9 and 2.9 MYA. This pattern supports a shift in net diversification rate, concordant with the expectations of the “colonization cycle” hypothesis, which implies a historical shift in dispersiveness among great speciator lineages during the evolutionary past. Here, we present a formalized framework that explains how repeated founder effects and shifting selection pressures on highly dispersive genotypes are the only ultimate causes needed to generate the paradox of the great speciators. Within this framework, we emphasize that lineage-specific traits and island-specific abiotic factors will result in varying levels of selection pressure against dispersiveness, caused by varying proximate eco-evolutionary mechanisms. Overall, we highlight how understanding patterns of diversification in the Ceyx dwarf kingfishers helped us generate a cohesive framework that provides a rigorous mechanistic explanation for patterns concordant with the paradox of the great speciators and the repeated emergence of geographic radiations in island archipelagoes across the globe.
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- Award ID(s):
- 2112467
- PAR ID:
- 10537983
- Publisher / Repository:
- Oxford
- Date Published:
- Journal Name:
- Evolution Letters
- ISSN:
- 2056-3744
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Hahn, Matthew (Ed.)Abstract The flora and fauna of island systems—especially those in the Indo-Pacific—are renowned for their exceptional diversification and for shaping key evolutionary theories. Yet, phylogenetic studies often undersample the full diversity of these geographic radiations. This gap stems both from the challenges of collecting single-island endemics and from the poor performance of degraded DNA when using museum specimens to infer evolutionary relationships. Advances in generating genome-wide data sets with degraded DNA from museum samples are overcoming these obstacles. Here, we leveraged 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 found that four types of molecular markers (UCEs, BUSCOs, SNPs, and mtDNA) and tree-building methods did not recover a single well-supported and concordant species-level topology. Instead, we revealed pervasive incomplete lineage sorting and both ancient and contemporary gene flow, processes contribute to conflicting evolutionary histories. Complete taxonomic sampling uncovered a novel case of mitochondrial discordance between two allopatric species, consistent with a historical (but since lost) hybrid zone during successive island colonizations. Together, these results underscore how dense genomic and taxonomic sampling can reveal complex evolutionary dynamics in rapid island radiations.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/evlett/qrae035
