Solving the paradox of the great speciator on the Solomon Islands

Rapid loss of dispersal might be key to explain rapid speciation on islands. 

Charles Darwin called the origin of new species “that mystery of mysteries”. And despite decades of intensive evolutionary research, there are still several unsolved questions on speciation. One of my personal favorites is “the paradox of the great speciators”. This conundrum – which would make a great movie title – refers to avian species complexes that occur on islands with different levels of geographic isolation: from narrowly separated to very remote islands. Each island has its own endemic and genetically differentiated population (sometimes considered distinct species or subspecies). This situation raises the question of how some species complexes can disperse over a wide area, often coming into secondary contact and experiencing consequent gene flow, and still rapidly give rise to new species. To solve this paradox, ornithologists have often turned to the White-eyes (family Zosteropidae). This group of birds can be found across the Old World, but also on the archipelagos of the Pacific Ocean where they diversified into numerous (sub)species. A recent study in the journal Evolution focused on White-eyes of the Solomon Islands to find an answer to the paradox of this great speciator.

An overview of the different Zosterops populations on the Solomon Islands. From: Manthey et al. (2020) Evolution.

 

Gene Flow Patterns

To understand how new White-eye species evolve on these islands, we need to know how isolated the different islands populations are from one another. Therefore, Joseph Manthey and his colleagues collected DNA samples across the Solomon Islands to reconstruct patterns of gene flow. Using the software TreeMix, the researchers were able to reconstruct the historical relationships between the island populations and pinpoint gene flow events (indicated with red arrows in the figure below). The findings from TreeMix were supported by other statistical tests, such as D-statistics.

Interestingly, these analyses suggested gene flow between distant populations, but not between nearby islands. For example, there has been gene flow between Grey-throated White-eye (Zosterops ugiensis) and Yellow-throated White-eye (Z. metcalfii) that are separated by at least 50 kilometers of deep waters. In contrast, species in the New Georgia Group, such as Vella Lavella White-eye (Z. vellalavella) and Ranongga White-eye (Z. splendidus), are only a few kilometers apart but do not exchange genetic material. Moreover, the populations on neighboring islands are genetically and morphologically distinct, indicating rapid evolution.

The TreeMix analysis shows the historical relationships between the island populations with several gene flow events (indicated with red arrows). From. Manthey et al. (2020) Evolution.

 

Loss of Dispersal

What can explain these peculiar patterns?  The researchers offer two explanations for the lack of gene flow between neighboring islands: (1) these species do not venture across the narrow straits, or (2) they do visit neighboring islands but they do not mix with the resident species due to differences in plumage or song which evolve rapidly. Because species from distant islands can still interbreed, the researchers argue that the first explanation (a loss in dispersal) is the most likely explanation for the gene flow patterns at nearby islands. After a highly dispersive phase of island colonization, the newly established populations would immediately experience strong selection for reduced dispersal.

I would add another aspect to this scenario. Perhaps the selection for reduced dispersal is related to reproductive isolation between different islands (explanation 2). Early in this process, dispersing individuals end up on neighboring islands and occasionally manage to interbreed with the resident species. However, the resulting hybrids fail to reproduce because their intermediate phenotype prevents them from finding a suitable mate. Over time, this selection against hybrids could strengthen reproductive isolation between the parental species (i.e. a process known as reinforcement). Later on, dispersing birds stop interbreeding with their neighbors, increasing selection against dispersing individuals. Whether this idea makes sense remains to be tested. But slowly we are getting closer to understanding rapid speciation on islands and solving the paradox of the great speciator.

 

References

Manthey, J. D., Oliveros, C. H., Andersen, M. J., Filardi, C. E., & Moyle, R. G. (2020). Gene flow and rapid differentiation characterize a rapid insular radiation in the southwest Pacific (Aves: Zosterops). Evolution74(8), 1788-1803.

Featured image: Warbling White-eye (Zosterops japonicus) © Obubu Interns

 

This paper has been added to the Zosteropidae page.

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