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Multiple aquatic invasions by an endemic, terrestrial Hawaiian moth radiation.

ABSTRACT: Insects are the most diverse form of life on the planet, dominating both terrestrial and freshwater ecosystems, yet no species has a life stage able to breath, feed, and develop either continually submerged or without access to water. Such truly amphibious insects are unrecorded. In mountain streams across the Hawaiian Islands, some caterpillars in the endemic moth genus Hyposmocoma are truly amphibious. These larvae can breathe and feed indefinitely both above and below the water's surface and can mature completely submerged or dry. Remarkably, a molecular phylogeny based on 2,243 bp from both nuclear (elongation factor 1alpha and carbomoylphosphate synthase) and mitochondrial (cytochrome oxidase I) genes representing 216 individuals and 89 species of Hyposmocoma reveals that this amphibious lifestyle is an example of parallel evolution and has arisen from strictly terrestrial clades at least three separate times in the genus starting more than 6 million years ago, before the current high islands existed. No other terrestrial genus of animals has sponsored so many independent aquatic invasions, and no other insects are able to remain active indefinitely above and below water. Why and how Hyposmocoma, an overwhelmingly terrestrial group, repeatedly evolved unprecedented aquatic species is unclear, although there are many other evolutionary anomalies across the Hawaiian archipelago. The uniqueness of the community assemblages of Hawaii's isolated biota is likely critical in generating such evolutionary novelty because this amphibious ecology is unknown anywhere else.

SUBMITTER: Rubinoff D

PROVIDER: S-EPMC2851915 | biostudies-literature | 2010 Mar

REPOSITORIES: biostudies-literature

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Multiple aquatic invasions by an endemic, terrestrial Hawaiian moth radiation.

Rubinoff Daniel D Schmitz Patrick P

Proceedings of the National Academy of Sciences of the United States of America 20100322 13

Insects are the most diverse form of life on the planet, dominating both terrestrial and freshwater ecosystems, yet no species has a life stage able to breath, feed, and develop either continually submerged or without access to water. Such truly amphibious insects are unrecorded. In mountain streams across the Hawaiian Islands, some caterpillars in the endemic moth genus Hyposmocoma are truly amphibious. These larvae can breathe and feed indefinitely both above and below the water's surface and ...[more]

PMID: 20308549

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Project description:Background"Explosive" adaptive radiations on islands remain one of the most puzzling evolutionary phenomena. The rate of phenotypic and ecological adaptations is extremely fast during such events, suggesting that many genes may be under fairly strong selection. However, no evidence for adaptation at the level of protein coding genes was found, so it has been suggested that selection may work mainly on regulatory elements. Here we report the first evidence that positive selection does operate at the level of protein coding genes during rapid adaptive radiations. We studied molecular adaptation in Hawaiian endemic plant genus Schiedea (Caryophyllaceae), which includes closely related species with a striking range of morphological and ecological forms, varying from rainforest vines to woody shrubs growing in desert-like conditions on cliffs. Given the remarkable difference in photosynthetic performance between Schiedea species from different habitats, we focused on the "photosynthetic" Rubisco enzyme, the efficiency of which is known to be a limiting step in plant photosynthesis.ResultsWe demonstrate that the chloroplast rbcL gene, encoding the large subunit of Rubisco enzyme, evolved under strong positive selection in Schiedea. Adaptive amino acid changes occurred in functionally important regions of Rubisco that interact with Rubisco activase, a chaperone which promotes and maintains the catalytic activity of Rubisco. Interestingly, positive selection acting on the rbcL might have caused favorable cytotypes to spread across several Schiedea species.SignificanceWe report the first evidence for adaptive changes at the DNA and protein sequence level that may have been associated with the evolution of photosynthetic performance and colonization of new habitats during a recent adaptive radiation in an island plant genus. This illustrates how small changes at the molecular level may change ecological species performance and helps us to understand the molecular bases of extremely fast rate of adaptation during island adaptive radiations.

Dataset Information

Multiple aquatic invasions by an endemic, terrestrial Hawaiian moth radiation.

Publications

Multiple aquatic invasions by an endemic, terrestrial Hawaiian moth radiation.

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