DeRaad Devon A, Files Alexandra N, DeCicco Lucas H, Martin Rene P, McCullough Jenna M, Holland Piokera, Pikacha Douglas, Tigulu Ikuo G, Boseto David, Lavery Tyrone H, Andersen Michael J, Moyle Robert G
Biodiversity Institute and Natural History Museum, University of Kansas, Lawrence, KS, United States.
Department of Ichthyology, Division of Vertebrate Zoology, American Museum of Natural History, New York, NY, United States.
Evol Lett. 2024 Jul 26;8(6):813-827. doi: 10.1093/evlett/qrae035. eCollection 2024 Dec.
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 . Here, using genomic sequencing and comprehensive geographic sampling of the monophyletic 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 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.
大物种形成者的悖论描述了大洋洲众多鸟类谱系所呈现的一种矛盾的生物地理模式。具体而言，这些谱系在该地区呈现出广泛的地理分布，这意味着它们具有很强的跨水扩散能力；然而，它们也表现出反复的遗传和表型分化——即使在地理上相邻的岛屿之间也是如此——这意味着岛屿间的扩散能力较差。最初被引为这一悖论证据的一个类群是 属的小型翠鸟。在这里，通过对来自美拉尼西亚北部的单系辐射进行基因组测序和全面的地理采样，我们发现了反复出现的、深度的遗传分化，并且在地理上相邻岛屿上发现的谱系之间没有基因流动的证据，这为大物种形成者的悖论提供了一个极其清晰的例子。一个有时间标定的系统发育重建表明，在距今390万至290万年前到达美拉尼西亚北部后，迅速发生了一次显著的多样化爆发。这种模式支持了净多样化率的转变，这与“殖民循环”假说的预期一致，该假说意味着在进化历史中，大物种形成者谱系的扩散性发生了历史性转变。在这里，我们提出了一个形式化的框架，解释了反复出现的奠基者效应以及对高度扩散基因型的选择压力变化是产生大物种形成者悖论所需的唯一终极原因。在这个框架内，我们强调谱系特异性特征和岛屿特异性非生物因素将导致由不同的近缘生态进化机制引起的对扩散性的选择压力水平不同。总体而言，我们强调了理解小型翠鸟的多样化模式如何帮助我们生成一个连贯的框架，该框架为与大物种形成者悖论以及全球岛屿群岛中地理辐射的反复出现相一致的模式提供了一个严谨的机制解释。
