Winston Max E, Kronauer Daniel J C, Moreau Corrie S
Committee on Evolutionary Biology, University of Chicago, Chicago, IL, 60637, USA.
Department of Science and Education, Integrative Research Center, Field Museum of Natural History, Chicago, IL, 60605, USA.
Mol Ecol. 2017 Feb;26(3):859-870. doi: 10.1111/mec.13846. Epub 2016 Oct 25.
The emergence of the Isthmus of Panama is one of the most important events in recent geological history, yet its timing and role in fundamental evolutionary processes remain controversial. While the formation of the isthmus was complete around 3 million years ago (Ma), recent studies have suggested prior intercontinental biotic exchange. In particular, the possibility of early intermittent land bridges facilitating colonization constitutes a potential mechanism for speciation and colonization before full closure of the isthmus. To test this hypothesis, we employed genomic methods to study the biogeography of the army ant genus Eciton, a group of keystone arthropod predators in Neotropical rainforests. Army ant colonies are unable to disperse across water and are therefore ideally suited to study the biogeographic impact of land bridge formation. Using a reduced representation genome sequencing approach, we show that all strictly Central American lineages of Eciton diverged from their respective South American sister lineage between 4 and 7 Ma, significantly prior to the complete closure of the isthmus. Furthermore, three of the lineage pairs form extensive and coincident secondary contact zones in Costa Rica and Nicaragua, with no evidence of gene flow. Such a discrete and repeated biogeographic pattern indicates at least two waves of army ant dispersal into Central America that were separated by significant genetic divergence times. Thus, by integrating phylogenomic, population genomic and geographic evidence, we show that early colonization of Central America across the emerging Isthmus of Panamá drove parallel speciation in Eciton army ants.
巴拿马地峡的出现是近代地质史上最重要的事件之一，但其形成时间及其在基本进化过程中的作用仍存在争议。虽然地峡的形成在约300万年前（Ma）就已完成，但最近的研究表明此前存在洲际生物交流。特别是，早期间歇性陆桥促进物种定殖的可能性构成了地峡完全闭合之前物种形成和定殖的一种潜在机制。为了验证这一假设，我们采用基因组方法研究了行军蚁属Eciton的生物地理学，该属是新热带雨林中的一类关键节肢动物捕食者。行军蚁群体无法跨越水域扩散，因此非常适合用于研究陆桥形成的生物地理影响。通过使用简化基因组测序方法，我们发现Eciton所有严格局限于中美洲的谱系在400万至700万年前与其各自的南美洲姊妹谱系分化，这明显早于地峡的完全闭合。此外，三对谱系在哥斯达黎加和尼加拉瓜形成了广泛且重合的次生接触带，没有基因流的证据。这种离散且重复的生物地理模式表明至少有两波行军蚁扩散到中美洲，且它们之间存在显著的遗传分化时间间隔。因此，通过整合系统发育基因组学、群体基因组学和地理证据，我们表明穿越新出现的巴拿马地峡向中美洲的早期定殖推动了Eciton行军蚁的平行物种形成。
