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.

Fig. 1.

Map of the Hawaiian Islands. The locations of collecting sites are indicated by yellow dots for terrestrial Hyposmocoma larvae and by blue dots for aquatic Hyposmocoma larvae.

Fig. 2.

Underwater activity of larvae representing each of the three amphibious case-bearing caterpillar lineages belonging to the endemic Hawaiian moth genus Hyposmocoma. (A) “Burrito”-shaped case larvae attached to substrate with silk line. (B) “Cone”-shaped case larvae feeding on algae. (C) “Bugle”-shaped case larvae crawling on submerged rocks. See SI for videos of larvae moving in and out of water (Movies S1 and S2).

Fig. 3.

Phylogeny of Hyposmocoma moths based on molecular data with the three lineages including amphibious species highlighted. Shown is the maximum likelihood tree based on combined analysis of three genes: the mitochondrial gene cytochrome oxidase subunit I and the nuclear genes elongation factor 1α and carbomoylphosphate synthase. Bayesian posterior probabilities ≥95 and nonparametric bootstrap supports ≥70 are given under each corresponding node and clade. This topology is congruent with the Bayesian topology (Fig. S3). Numbers on the right of the different terrestrial clades represent species per clade, with blue numbers in brackets representing total of aquatic species. Proportional likelihoods of ancestral states are mapped onto each node of interest (red = terrestrial; blue = aquatic); exact values are given in Fig. S6. Branch lengths are drawn to scale, as indicated by scale bars.

Fig. 4.

Maximum clade credibility chronogram inferred using the uncorrelated relaxed clock model of rate evolution. Error bars represent 95% posterior credibility intervals and are only given for nodes that were present on more than 50% of the posterior sampled trees. Red filled circles represent the two nodes used for calibration. Ages are given in millions of years before present.