Department of Ecology, Behavior and Evolution, School of Biological Sciences, University of California San Diego, La Jolla, California, USA.
Smithsonian Tropical Research Institute, Ancon, Balboa, Panama.
Appl Environ Microbiol. 2024 Nov 20;90(11):e0100324. doi: 10.1128/aem.01003-24. Epub 2024 Oct 31.
The rise of the Isthmus of Panama separated the populations of many marine organisms, which then diverged into new geminate sister species currently living in the Eastern Pacific Ocean and the Caribbean Sea. However, we know very little about how such evolutionary divergences of host species have shaped the compositions of their microbiomes. Here, we compared the microbiomes of whole-body and shell-surface samples of geminate species of marine gastropods in the genera and to those of congeneric outgroups. Our results suggest that the effects of ~3 million years of separation and isolation on microbiome composition varied among host genera and between sample types within the same hosts. In the whole-body samples, microbiome compositions of geminate species pairs tended to be similar, likely due to host filtering, although the strength of this relationship varied among the two groups and across similarity metrics. Shell-surface microbiomes show contrasting patterns, with co-divergence between the host taxa and a small number of microbial clades evident in but not . These results suggest that (i) isolation of host populations after the rise of the Isthmus of Panama affected microbiomes of geminate hosts in a complex and host-specific manner, and (ii) host-associated microbial taxa respond differently to vicariance events than the hosts themselves.IMPORTANCEWhile considerable work has been done on evolutionary divergences of marine species in response to the rise of the Isthmus of Panama, which separated two previously connected oceans, how this event shaped the microbiomes of these marine hosts remains poorly known. Using whole-body and shell-surface microbiomes of closely related gastropod species from opposite sides of the Isthmus, we show that divergences of microbial taxa after the formation of the Isthmus are often not concordant with those of their gastropod hosts. Our results show that evolutionary responses of marine gastropod-associated microbiomes to major environmental perturbations are complex and are shaped more by local environments than host evolutionary history.
巴拿马地峡的崛起将许多海洋生物的种群分隔开来，这些种群随后分化为新的双生姐妹种，目前分别生活在东太平洋和加勒比海。然而，我们对宿主物种的这种进化分歧如何影响其微生物组的组成知之甚少。在这里，我们比较了双生海洋腹足纲动物属和属的整体样本和壳表面样本的微生物组与同属外群的微生物组。我们的结果表明，大约 300 万年的隔离和分离对微生物组组成的影响因宿主属的不同而不同，也因宿主内的不同样本类型而不同。在整体样本中，双生种对的微生物组组成往往相似，这可能是由于宿主的过滤作用，尽管这种关系的强度在两组和跨相似性度量标准上有所不同。壳表面微生物组显示出相反的模式，在属中宿主分类单元之间存在共同进化，并且在 中而不是 中存在少数微生物类群。这些结果表明：(i)巴拿马地峡崛起后宿主种群的隔离以复杂且宿主特异性的方式影响了双生宿主的微生物组；(ii)与宿主本身相比，宿主相关的微生物分类群对隔离事件的反应不同。
重要性尽管已经对由于巴拿马地峡的崛起而导致的海洋物种的进化分歧进行了大量研究，该事件将两个以前相连的海洋分隔开来，但这种事件如何塑造这些海洋宿主的微生物组仍知之甚少。我们使用来自地峡两侧的密切相关的腹足纲动物的整体样本和壳表面微生物组，表明地峡形成后微生物类群的分歧通常与它们的腹足纲宿主的分歧不一致。我们的研究结果表明，海洋腹足纲动物相关微生物组对重大环境干扰的进化反应是复杂的，更多地受到局部环境的影响，而不是宿主进化史的影响。
