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Ancient Diversification of Hyposmocoma Moths in Hawaii

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Ancient Diversification of Hyposmocoma Moths in Hawaii ARTICLE Received 29 Jul 2013 | Accepted 20 Feb 2014 | Published 20 Mar 2014 DOI: 10.1038/ncomms4502 Ancient diversification of Hyposmocoma moths in Hawaii William P. Haines1, Patrick Schmitz1 & Daniel Rubinoff1 Island biogeography is fundamental to understanding colonization, speciation and extinction. Remote volcanic archipelagoes represent ideal natural laboratories to study biogeography because they offer a discrete temporal and spatial context for colonization and speciation. The moth genus Hyposmocoma is one of very few lineages that diversified across the entire Hawaiian Archipelago, giving rise to over 400 species, including many restricted to the remote northwestern atolls and pinnacles, remnants of extinct volcanoes. Here, we report that Hyposmocoma is B15 million years old, in contrast with previous studies of the Hawaiian biota, which have suggested that most lineages colonized the archipelago after the emergence of the current high islands (B5 Myr ago). We show that Hyposmocoma has dispersed from the remote Northwestern Hawaiian Islands to the current high islands more than 20 times. The ecological requirements of extant groups of Hyposmocoma provide insights into vanished ecosystems on islands that have long since eroded. 1 University of Hawaii at Manoa, Department of Plant and Environmental Protection Sciences, 3050 Maile Way, Gilmore 310, Honolulu 96822, Hawaii, USA. Correspondence and requests for materials should be addressed to D.R. (email: [email protected]). NATURE COMMUNICATIONS | 5:3502 | DOI: 10.1038/ncomms4502 | www.nature.com/naturecommunications 1 & 2014 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms4502 ne of the most intriguing challenges in biology is the in a much drier, less productive, archipelago that no longer development of a timescale and robust paradigm for the supported diverse forest habitats or the organisms that depended Oprocess of speciation. Volcanic islands represent ideal on them. This theory depends partly on climatic patterns, which study systems since they are impermanent platforms for can vary considerably on the scale of thousands, let alone millions evolution; as soon as the building phase is complete, they subside of years6. In addition to the lack of high mountains, there were back into the ocean, eroding slowly until they disappear beneath two periods during which emerging islands were much more the waves. Because of this dynamic process, endemic species distantly spaced than at other times: 27–28 Myr ago and 5–7 Myr radiations on remote volcanic islands are unique models for ago (just before the formation of Kauai, the oldest of the current understanding the chronology of diversification in the framework high islands) (Fig. 1). When Kauai formed, there were only of an isolated geological setting1. relatively small, low islands available as sources, and the largest of The Hawaiian Archipelago is the most isolated island chain on these (Nihoa, Necker, LaPerouse and Gardner) were relatively Earth, and is renowned as a site for the study of biogeography and distant compared with the spacing of the present high islands2. speciation, in large part due to its remarkable geological history. Thus, it is thought that distance and limited habitat variability on All of its islands formed over a volcanic hotspot in the central the source islands caused a ‘bottleneck’ that resulted in severe Pacific, but as the Pacific plate carries them to the northwest, they attrition in ancient lineages. move away from the relatively stationary source of magma. Once Evidence from molecular clock studies generally supports this cut off from the magma, the islands gradually subside back into claim; Price and Clague2 reviewed phylogenetic studies of the ocean, becoming ever smaller rocky islets, pinnacles and Hawaiian plant and animal lineages, and found that the vast finally coral atolls over the course of tens of millions of years. majority of age estimates were younger than the age of Kauai. Thus, the islands are ordered linearly by age (Fig. 1)2. The This suggests that most endemic lineages that formerly occurred established ages of the islands, in concert with recent molecular on the oldest islands did not persist, and diminishes the role that clock advances, facilitate increasingly accurate time estimates these atolls and pinnacles played in generating the archipelago’s of past speciation events. They provide powerful tools for present diversity, despite their greater size in the distant past. unravelling the evolutionary history and impacts of geology on Only four extant lineages of plants or animals7–10 are thought to insular species radiations3–5. While the relatively young current have colonized the Hawaiian archipelago before the emergence of high islands range in age from 0.5 (island of Hawaii) to 4.7 Myr Kauai, but since all the living species in these apparently ancient ago (island of Kauai), the oldest of the persisting Northwestern lineages are currently restricted to the youngest islands, prior Hawaiian Islands (NWHI), Kure atoll, is estimated at 29.8 Myr residence in the Hawaiian chain can only be inferred based on ago2,3. These ancient islands, some of which in their prime, divergence time estimates. Moreover, very few of today’s species rivalled the current high islands in size and topographic diversity, radiations have extant representatives on the NWHI, implying greatly extend the temporal window theoretically available for widespread extinction of ancient groups that never reached the insular evolution in the Hawaiian Archipelago2. younger islands, and thus extensive lineage turnover between However, the formation of the NWHI over the past 20 Myr ago islands greater than and those less than 5 Myr old. Understanding was temporally inconsistent, which may have limited the survival patterns of diversification in an ancient lineage would provide and dispersal of ancient lineages2,3. By the time Kauai was formed a unique perspective on the influence of time on island B5 Myr ago, it is thought that few (if any) of the older islands biogeography. had peaks over 1,000 m in elevation2. It is assumed that low The endemic Hawaiian moth genus Hyposmocoma is one of very elevations severely limited precipitation on these islands, resulting few groups that maintain multiple single-island endemic species Kure (29.8 Ma) Midway (28.7 Ma) Lisianski N (23.4 Ma) Direction of plate movement Laysan (20.7 Ma) Gardner (15.8 Ma) LaPerouse (12.8 Ma) Necker (11.0 Ma) Nihoa (7.3 Ma) Kauai and Niihau (5.1–4.7 Ma) Reduced volcanic 0 200 400 600 800 1,000 km Maui Nui complex activity (2.2–1.2 Ma) Oahu Hawaii (3.0–2.6 Ma) (0.5–0 Ma) Figure 1 | Map of the Hawaiian Archipelago. Filled black areas represent current coastlines, while grey areas represent the maximum historical above-water island area. White dots correspond to volcanoes, peaks or small islands that are currently above sea level, while black dots indicate submerged seamounts. Note the lack of large islands between the islands of Necker (formed about 11.0 Myr ago) and Kauai and Niihau (formed 5.1–4.7 Myr ago). Figure reproduced with permission from the publisher, The Royal Society2. 2 NATURE COMMUNICATIONS | 5:3502 | DOI: 10.1038/ncomms4502 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms4502 ARTICLE across the entire archipelago, including the NWHI. As such, this Here we investigate the evolutionary history of this group, and genus provides an unparalleled opportunity to examine the its colonization patterns across the archipelago, using a systematic evolutionary history and island biogeography of an old, endemic framework and molecular clock estimates from five genes, radiation. Of particular interest, a group like Hyposmocoma offers a calibrated based on the geological history of the Hawaiian chance to include the role of the dwindling, ancient islands, many Islands. We report that Hyposmocoma is an ancient lineage, of which maintain their own endemic species. having diversified in the NWHI, and dispersed more than Hyposmocoma is a monophyletic radiation containing over 20 times to the current high islands. 400 estimated species and accounting for one third of all butterfly 11 and moth diversity in the Hawaiian Islands . It represents one Results of the most spectacular and species-rich endemic radiations in Phylogenetic relationships. The molecular phylogeny of the archipelago, second in numbers only to the Hawaiian Hyposmocoma recovers strongly supported species groups that, Drosophilidae, which are largely restricted to relatively mesic for the most part, correspond to nine distinct case types included habitats in the current high islands12. In contrast, Hyposmocoma in our analysis (Fig. 2). The phylogeny supports the division occur on virtually every emergent landmass in the archipelago, of the genus Hyposmocoma into two previously recognized and each species appears to be endemic to a single island. subgenera: Euperissus, whose larvae do not build cases, and The moths have diversified into a wide range of habitats, from Hyposmocoma sensu stricto, whose larvae build elaborate cases11. xeric lava fields along the ocean to high elevation bogs, fostering The basal lineages of Hyposmocoma sensu stricto have caterpillars many novel adaptations, including unique amphibious13 and that build cases with two entrances, one on each side, while a carnivorous14 case-making caterpillars. While many species of derived
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