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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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Consistent accumulation of transposable elements in species of the Hawaiian Tetragnatha spiny-leg adaptive radiation across the archipelago chronosequence
Abstract The ecological and phenotypic diversity observed in oceanic island radiations presents an evolutionary paradox: a high level of genetic variation is typically required for diversification, but species colonizing a new island commonly suffer from founder effects. This reduction in population size leads to lower genetic diversity, which ultimately results in a reduction in the efficiency of natural selection. What then is the source of genetic variation which acts as the raw material for ecological and phenotypic diversification in oceanic archipelagos? Transposable elements (TEs) are mobile genetic elements that have been linked to the generation of genetic diversity, and evidence suggests that TE activity and accumulation along the genome can result from reductions in population size. Here, we use the Hawaiian spiny-leg spider radiation (Tetragnatha) to test whether TE accumulation increases due to demographic processes associated with island colonization. We sequenced and quantified TEs in 23 individuals representing 16 species from the spiny-leg radiation and four individuals from its sister radiation, the Hawaiian web-building Tetragnatha. Our results show that founder effects resulting from colonization of new islands have not resulted in TE accumulation over evolutionary time. Specifically, we found no evidence for an increase in abundance of specific TE superfamilies, nor an accumulation of ‘young TEs’ in lineages which have recently colonized a new island or are present in islands with active volcanoes. We also found that the DNA/hAT transposon superfamily is by far the most abundant TE superfamily in the Tetragnatha radiation. This work shows that there is no clear trend of increasing TE abundance for the spiny-leg radiation across the archipelago chronosequence, and TE accumulation is not affected by population oscillations associated with island colonization events. Therefore, despite their known role in the generation of genetic diversity, TE activity does not appear to be the mechanism explaining the evolutionary paradox of insular diversification in the Tetragnatha spiny-leg radiation.
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- Award ID(s):
- 1927510
- PAR ID:
- 10540746
- Publisher / Repository:
- Linnean Society
- Date Published:
- Journal Name:
- Evolutionary Journal of the Linnean Society
- Volume:
- 3
- Issue:
- 1
- ISSN:
- 2752-938X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/evolinnean/kzae005
