Journal of Biogeography (J. Biogeogr.) (2016)
SYNTHESIS Molecular phylogeography of the Society Islands (Tahiti; South Pacific) reveals departures from hotspot archipelago models David H. Hembry1,2,3* and Brad Balukjian4
1Center for Ecological Research, Kyoto ABSTRACT University, Otsu, Shiga, Japan, 2Department Aim Phylogeographical and modelling studies have suggested that the biotas of of Molecular and Cell Biology, University of 3 oceanic hotspot archipelagos (such as the Hawaiian, Canary and Gal apagos California, Berkeley, CA, USA, Department of Ecology and Evolutionary Biology, islands) diversify in parallel with the formation of the islands on which they University of Arizona, Tucson, AZ, USA, live. Here, we review the phylogeography of the native terrestrial biota of the < 4Department of Biology, Laney College, Society Islands, an archipelago formed 4.6 Ma, to test this model. Oakland, CA, USA Location Society Islands, French Polynesia (Pacific Ocean). Methods We reviewed 49 phylogenetic and phylogeographical studies incor- porating Society Island terrestrial animal and plant taxa. We ask: (1) Where are the sister groups of Societies lineages distributed? (2) Are Societies-endemic ‘radiations’ monophyletic or polyphyletic? (3) What between-island barriers are seen in the phylogeography of Societies taxa? (4) What within-island barriers are seen in the phylogeography of Societies taxa? (5) How old is the Societies biota? Results Most Societies lineages are closely related to those in other tropical Pacific archipelagos, particularly the Cook, Austral and Marquesas Islands (< 2000 km distant). More genera show strong evidence for polyphyly (13 gen- era) than for monophyly (4 genera) in the Society Islands. The most common within-archipelago phylogeographical barrier corresponds to the straits (150 km) between the Windward Society and Leeward Society Islands. Only a few groups, primarily species-rich invertebrate radiations, show divergence among or within islands. Published divergence time estimates suggest that much of the Societies biota may be much younger than the age of the archipe- lago.
Main conclusions Much of the Societies biota does not appear to have diver- sified in parallel with the formation of the archipelago, differing from ‘progres- sion rule’ and general dynamic models for the diversification of oceanic archipelago biotas. Rather, many Societies ‘radiations’ may have been assem- bled via repeated, independent colonizations, which may have entailed exten- sive macroevolutionary turnover of colonizing lineages. These patterns have implications for the biogeography of other Pacific hotspot archipelagos. *Correspondence: Dr. David H. Hembry, University of Arizona, Department of Ecology Keywords and Evolutionary Biology, P.O. Box 210088, oceanic hotspot archipelago, Pacific, phylogeography, repeated colonization, Tucson, AZ 85721, USA E-mail: [email protected] Society Islands, Tahiti
Tahiti, Bora Bora and Moorea, are an oceanic archipelago INTRODUCTION formed by volcanoes in the central South Pacific. However, The Society Islands have loomed large in the Western imagi- despite an early visit by Darwin (1839), and extensive ende- nation since first contact between Tahitians and Europeans mism in their biota (Meyer, 2004), they have received less in 1767. These islands, of which the most famous are attention from evolutionary biologists than other oceanic
ª 2016 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 1 doi:10.1111/jbi.12723 D. H. Hembry and B. Balukjian
(a)
Northwest Hawaiian Is. 7.2−27.7 Ma
Main Hawaiian Is. 0−5.1 Ma
Samoa Marquesas 0−2.3 Ma Society Is. 1.3−5.5 Ma 0−4.6 Ma
Rarotonga (Cooks) Gambier Is.−Pitcairn Is. 1.4 Ma Austral Is. 0.6−5.8 Ma 3.8−9.1 Ma −40 −20 0 20 40
140 160 180 −160 −140 −120 −100 (b)
Tikehau Figure 1 Maps of Pacific Basin and Society Rangiroa TUAMOTU Islands. (a) Pacific Basin, indicating location Makatea Motu One ISLANDS of the Society Islands and other archipelagos Tupai mentioned in text. (b) Society Islands. The Maupiti Tahaa Societies are divided geographically and Manuae Bora Bora Huahine Tetiaroa administratively into the Leeward (Maupiti, Maupihaa Raiatea Tupai, Bora Bora, Tahaa, Raiatea, Huahine, LEEWARD ISLANDS Moorea Tahiti Nui Maupihaa, Motu One, Manuae) and the Taiarapu Windward (Maiao, Moorea, Tetiaroa, Maiao (Tahiti Iti) Tahiti Mehetia Tahiti, Mehetia) Islands. Tahiti is WINDWARD ISLANDS dominated by two volcanoes (Tahiti Nui and Tahiti Iti/Taiarapu) connected by an 0 100 200 km isthmus. The 150 km wide straits between
−19 −18 −17 −16 −15 the Windwards and Leewards are the most important phylogeographical barrier in −154 −152 −150 −148 Societies taxa. archipelagos such as the Hawaiian, Gal apagos and Macarone- community assembly and macroevolutionary diversification sian islands. dynamics (Darwin, 1859; MacArthur & Wilson, 1967; Car- The Society Islands are one of several linear hotspot archi- lquist, 1974; Coyne & Orr, 2004; Grant & Grant, 2008; Gille- pelagos on the Pacific Plate, along with the Hawaiian, Mar- spie & Baldwin, 2009). quesas, Cook-Austral and Samoan islands (Fig. 1a). All these Extensive phylogenetic study of the biota of Hawaii has archipelagos were likely formed by stationary hotspots under suggested that the linear age progression of its islands drives the Pacific Plate (Clouard & Bonneville, 2005). All have common phylogeographical patterns in the diversification of roughly the same orientation, with an age progression of its biota (Wagner & Funk, 1995; Roderick & Gillespie, 1998; youngest islands at the south-east end of the archipelago and Cowie & Holland, 2008; Gillespie & Baldwin, 2009). The the oldest at the north-west end; the existing high islands of most widely emphasized aspect of this model is termed the many of these archipelagos are less than or equal to 5 Myr ‘progression rule’, in which an endemic clade radiates in par- in age (Duncan & McDougall, 1976; Clouard & Bonneville, allel with the sequential formation of the islands (Wagner & 2005). Because these and other oceanic archipelagos are Funk, 1995). This implies that earlier diverging (more formed de novo by volcanism, their biotas are assembled ‘basal’) lineages are found on older islands and later diverg- entirely via long-distance dispersal and in situ diversification. ing (more ‘derived’) lineages are found on younger islands, They thus have long been considered laboratories for and that many of these radiations are similar in age to the studying processes such as speciation, adaptive radiation, archipelago itself (5.1 Ma for the main Hawaiian Islands). In
2 Journal of Biogeography ª 2016 John Wiley & Sons Ltd Society Islands phylogeography addition, many Hawaiian radiations show other common Table 1 Ages (intervals of active volcanism), areas and patterns. Most, even the most species-rich ones, are mono- maximum elevations of the high Society Islands (e.g. those phyletic. Furthermore, evidence for both between- and islands which are not atolls). Tahiti is composed of three within-island speciation is seen, due to the large size of volcanoes. Ages compiled from Diraison et al. (1991), Hildenbrand et al. (2004), Guillou et al. (2005) and Uto et al. islands, the fact that many islands are made of multiple vol- (2007). canoes and the distances between islands. Similar patterns have been reported in other well-studied oceanic archipela- Age Area Maximum 2 gos (Canaries and Gal apagos; Juan et al., 2000; Parent et al., Island Sub-archipelago (Ma) (km ) elevation (m) 2008), and have inspired highly influential conceptual mod- Maupiti Leeward 4.2–4.6 8 380 els for the way in which island ontogeny governs the diversi- Bora Bora Leeward 3.1–3.5 29 727 fication of insular biotas, such as the general dynamic model Tahaa Leeward 2.6–3.3 90 590 (Whittaker et al., 2008) and the overshoot hypothesis (Gille- Raiatea Leeward 2.4–2.8 168 1017 spie & Baldwin, 2009). Huahine Leeward 2.1–2.7 75 669 – Whether these conceptual models or elements thereof Maiao Windward 1.7 1.9 8.8 154 Moorea Windward 1.3–1.8 134 1207 apply to the diversification of the biotas of other Pacific Tahiti Windward 0.3–1.3 1045 2241 Plate hotspot archipelagos remains unclear and in some Mehetia Windward 0.0–0.3 2.3 435 cases, contentious because these island groups are much smaller in total area than the Hawaiian Islands and are much less isolated from each other. They also lack the elevational, 149–152° W (Fig. 1a,b). They are likely formed by the activ- climatic and topographic complexity of the Hawaiian archi- ity of a stationary hotspot under the Pacific Plate, leading to pelago. Taxonomists have long noted that these islands have aSW–NE gradient in island age from the youngest high fewer and smaller endemic radiations (radiations composed island, Mehetia (0.0–0.3 Ma, 2.3 km2; Diraison et al., 1991) entirely of locally endemic species), and less ecological diver- to the oldest high island, Maupiti (4.2–4.5 Ma, 8 km2; Blais sity within these radiations, than is the case in Hawaii (see et al., 2002; Guillou et al., 2005; Uto et al., 2007; Table 1; summary in Keast, 1996). Consequently, some authors (in Fig. 2). Collectively, the western set of islands (Maupiti, Bora the absence of phylogenetic data) have argued that within Bora, Tahaa, Raiatea, Huahine, Tupai, Maupihaa, Motu One the Pacific, Hawaii is a ‘special case’ in which the large size, and Manuae) are classified as the Leeward Islands (Raro- topography, spatial arrangement and isolation of its islands mata’i in Tahitian or ^Iles-sous-le-Vent in French), and the permit such spectacular radiation (Keast, 1996; Hembry eastern set (Moorea, Tahiti, Maiao, Tetiaroa, Mehetia) as the et al., 2013b). Conversely, other authors have argued based Windward Islands (Ni’amata’i in Tahitian or ^Iles-du-Vent in on phylogenetic data that particular radiations on other Paci- French). This age progression and the division of the archi- fic archipelagos (Societies: Bradley, 2003; Marquesas: Cibois pelago into two ‘subarchipelagos’ suggest two hypotheses for et al., 2004; Australs: Garb & Gillespie, 2006) show progres- between-island patterns in the diversification of the Societies sion rule patterns, potentially due to the same underlying biota (Fig. 3). In the first (Fig. 3a), branching order may fol- geological mechanisms as in Hawaii. No comprehensive phy- low the age progression of the islands in a progression rule, logeographical synthesis of any of these other archipelagos and in the second (Fig. 3b), Leeward and Windward taxa has been conducted (but see Gillespie et al., 2008). may form separate clades. Here we perform the first phylogeographical synthesis of The largest island, Tahiti, is made up of three volcanoes the Society Islands terrestrial biota (vascular flora and fauna). (Tahiti Nui, Taravao and Taiarapu/Tahiti Iti). The subaerial Among Pacific Plate hotspot archipelagos, the biodiversity portions of Tahaa, Raiatea, Huahine, Moorea and Tahiti Nui and phylogeography of this archipelago is the next-best-stu- are thought to have been formed in a three-stage process, died after Hawaii. We ask the following questions: (1) Where with an initial period of volcanism, followed by caldera col- are the sister groups of Societies lineages distributed? (2) Are lapse, followed by additional lava flows (Diraison et al., Societies-endemic radiations monophyletic or polyphyletic? 1991). In the case of Tahiti Nui, the volcanic activity is (3) What major between-island phylogeographical patterns thought to have been continuous from 1.3 Ma to at least are seen in Societies taxa? (4) What within-island phylogeo- 0.5 Ma, punctuated by two caldera collapses (one each on graphical patterns are seen in the Societies? (5) How old is the north and south sides of the volcano) between 0.87 and the Societies biota? Finally, we compare these findings to 0.85 Ma, resulting in subaerial and submarine landslides those from other Pacific hotspot archipelagos, particularly (Hildenbrand et al., 2004, 2006); erosion and the formation Hawaii. of deep valleys has taken place over 0.5 Ma to the present (Hildenbrand et al., 2008). These processes could potentially drive within-island diversification, particularly within Tahiti. GEOLOGY AND BIODIVERSITY OF THE SOCIETY The high islands of the Society Islands therefore overlap in ISLANDS age (0–4.6 Ma) with many other midplate, linear volcanic The Society Islands, politically part of French Polynesia, are archipelagos and islands on the Pacific Plate (Fig. 1a; located in the central south Pacific at roughly 16–18° S, Clouard & Bonneville, 2005). However, they are younger
Journal of Biogeography 3 ª 2016 John Wiley & Sons Ltd D. H. Hembry and B. Balukjian 1000 1500 2000 2500 Elevation (m) Elevation 0 500
Figure 2 Cartoon representing the chronological sequence of the Society Islands. Y-axis indicates maximum elevation at the present-day, and x-axis indicates Tahiti 0−0.3 Tahaa Maiao intervals of active volcanism for each island. Maupiti 4.2−4.6 2.6−3.3 2.4−2.8 1.3−1.8 0.3−1.3 3.1−3.5 2.1−2.7 1.7−1.9 Moorea Raiatea Mehetia Huahine
Bora Bora Bora Sizes and spacing of islands not to scale; atolls (Tupai, Tetiaroa, Maunae, Motu One, Island name and age (Ma) Maupihaa) omitted. than the Austral and Northwest Hawaiian islands (Clouard and ferns are diverse and major components of the flora; & Bonneville, 2005). Unsampled seamounts to the west of angiosperms show high levels of endemism with some nota- the Societies, if part of the same alignment, would date to 7– ble endemic radiations; native conifers are absent (Florence, 8 Ma, but whether or not they were ever subaerial is unclear 1997). Terrestrial arthropods are mostly small-bodied, with (Duncan & McDougall, 1976; Clouard & Bonneville, 2005); notable exceptions (cicada, dragonflies; Nishida, 2008). Smal- this is in contrast to the long history of subaerial islands in ler bodied insects usually show high levels of endemism, with the Hawaiian archipelago (Price & Clague, 2002). As a result, some spectacular endemic radiations (Craig & Curie, 1999; it is unclear whether the Societies could have been colonized Claridge, 2006; Liebherr, 2012, 2013; Balukjian, 2013; Even- by any terrestrial organisms prior to the emergence of Mau- huis, 2013) but also evidence for human-induced extinction piti 4.6 Ma. The closest archipelagos at the present time to (Kahn et al., 2015b). Where introduced predators are rare, the Societies are the Tuamotus (≥ 220 km), the Australs several species of land crabs are common at low elevations. (≥ 550 km) and the southern Cooks (≥ 680 km). Freshwater fishes and decapod crustaceans are restricted to The Societies vary greatly in maximum elevation and con- species which are either catadromous or are descended from sequently in habitat diversity (Fig. 4). The largest and sec- catadromous ancestors (Keith et al., 2002). Terrestrial gas- ond-youngest island, Tahiti, is nearly twice as high (2241 m) tropods are highly diverse with some major endemic radia- as the next highest islands (Moorea, 1207 m; Raiatea, tions, but have suffered extensive human-induced extinction 1017 m); it has a far greater area of montane cloud forest (Lee et al., 2014). Native terrestrial vertebrates are restricted than any other island (Meyer, 2010). Greater areas of high- to birds, and among these, human-induced extinction has elevation habitat presumably existed on Tahiti and older been extensive (Steadman & Pahlavan, 1992; Steadman, islands in the geological past but have since eroded away 2006). Of the terrestrial birds which remain extant, many (Hildenbrand et al., 2004). Similarly to other Pacific archipe- appear to have been historically endemic to the Societies, but lagos, the south-eastern side of all islands is the wetter, wind- evidence for endemic radiations is limited (Steadman, 2006). ward side and the north-west side is the drier, leeward side. Although most authors consider all species of terrestrial rep- Before human colonization, all these islands were covered by tiles to be introduced (Steadman, 2006), one species of gecko wet or mesic tropical forest, or cloud forest at higher eleva- may be native (but not endemic; Fisher, 1997). Many native tions (Meyer, 2004). Low elevations on all these islands have species of ferns, angiosperms (particularly strand plants), ter- been greatly transformed by human impacts beginning with restrial crabs and seabirds are widely distributed in the tropi- Polynesian colonization ≥ 1000 bp and accelerating with cal Pacific. Western colonialism and the introduction of invasive plants and livestock (Meyer, 2004; Kahn et al., 2015a,b). Conse- BIOGEOGRAPHICAL AFFINITIES OF SOCIETIES quently, the lowest high islands (Maupiti: 380 m; Maiao: TAXA 154 m; Mehetia: 435 m) retain almost no original vegetation (Meyer, 1999, 2007; Meyer et al., 2009). We compiled phylogenetic studies that include Society Like that of many other Pacific archipelagos, the native Islands taxa (see Appendix S1 in Supporting Information, terrestrial biota consists entirely of taxa whose ancestors were Fig. 5; including Wright et al., 2001; Gemmill et al., 2002; able to colonize by over-water dispersal (Fig. 5). Bryophytes Howarth et al., 2003; Tronchet et al., 2005; Swenson et al.,
4 Journal of Biogeography ª 2016 John Wiley & Sons Ltd Society Islands phylogeography
(a) from published phylogenies. Polyphyletic assemblages were considered as separate clades whenever possible. Sister relationships of Society Island taxa are varied, but cur- rent data indicate that they are entirely restricted to other archipelagos within the Pacific, Australia and New Zealand (Fig. 6a). Out of 44 Societies clades examined, a majority of both plant (14/23) and animal (17/21) lineages show sister- group relationships with taxa on oceanic archipelagos in the Pacific (south-eastern Polynesia, Samoa or Hawaii; Fig. 6c,d). Just under half of plant lineages (11/23) but a large majority of animal lineages (15/21) show sister-group relationships with taxa in other archipelagos within south-eastern Polynesia (the southern Cook, Austral, Tuamotu, Marquesas, Gambier or Pit- cairn Islands). The unevenness of sampling across Pacific archipelagos in these studies suggests that relationships within south-eastern Polynesia are likely underestimated for plants (e.g. in Cyrtandra, Psychotria). The largest number of taxa show sister-group affinities to the Cook Islands (13 taxa), the (b) Austral Islands (12 taxa) or the Marquesas Islands (9 taxa). When only studies are considered in which taxon sampling both inside and outside the Societies is considered ‘extensive’ or ‘comprehensive’ (13 studies total), the greatest number of lineages show affinities with the Cooks (7 taxa), Marquesas (4 taxa) and Australs (3 taxa), although these examples are domi- nated by angiosperms and birds (Fig. 6b). Nine plant lineages show sister relationships with western Polynesian archipelagos (Samoa, Futuna, Tonga or Fiji), whereas no Societies animal clades have western Polynesian taxa as their closest relatives outside the archipelago. Three plant taxa are found to be nested within (Astelia, Fuschia)or sister to (Melicope) New Zealand clades (Berry et al., 2004; Figure 3 Two phylogenetic hypotheses for Society Islands taxa. Harbaugh et al., 2009; Birch & Keeley, 2013), although no (a) Progression rule hypothesis in which the sequence of animals show relationships with New Zealand taxa. In con- divergence of lineages on islands corresponds to the ages of the trast, two animal lineages (Bembidion beetles and Coridro- islands (similar to a pattern widely reported on other oceanic mius bugs) show sister relationships with Australian taxa archipelagos). (b) Hypothesis in which the straits between the (Liebherr & Maddison, 2013; Tatarnic & Cassis, 2013), Windward and Leeward Society Islands drive divergence, without reference to island ages. whereas no plant lineages do. One bird species (the critically endangered Tahiti Monarch Pomarea nigra) is apparently 2007; Percy et al., 2008; Rundell et al., 2008; Balke et al., most closely related to species from Micronesia (Andersen 2009; Goodman & O’Grady, 2013; Goodman et al., 2014) et al., 2015a). with the aim of assessing the biogeographical distribution of These studies also reveal a number of cases in which Soci- their closest relatives. Many genera or species are poly- eties taxa are not sister to congeners on other high islands in phyletic or paraphyletic within the Societies, whereas others south-eastern Polynesia, indicating that different archipelagos are monophyletic. We thus ascertained the ‘closest relatives’ in this region were likely colonized independently. In plants, of Societies taxa as either the taxa which, together with Soci- particularly good examples of this are Astelia (Birch & Keeley, eties taxa, form a monophyletic group or the closest sister 2013), Psychotria (Barrab e et al., 2014), Coprosma (Cantley group to a monophyletic clade. In cases where node support et al., 2014) and Melicope (Harbaugh et al., 2009). In animals, values and phylogenetic relationships allow it to be unam- Ptilinopus fruit doves are perhaps the best-supported example biguous and useful, we also note the biogeographical distri- (Cibois et al., 2014); Tetragnatha spiders (Casquet et al., 2015) bution of the sister group to the larger clade containing and Pomarea monarchs (Andersen et al., 2015a) are other Societies taxa and their closest relatives (see Appendix S1). likely examples. As has been previously argued (Gillespie, Because taxon sampling varies across studies, we indicate the 2002; Garb & Gillespie, 2006), these examples suggest that comprehensiveness of taxon sampling inside and outside the independent colonizations of adjacent archipelagos are com- Society Islands. We did not include lineages (or studies) for mon in Pacific biogeography. which limited taxon sampling, a deeply basal position in the Finally, Tahiti has a number of ‘unique’ lineages whose tree, or poor support values make sister relationships unclear closest relatives are distant from the Societies. These include
Journal of Biogeography 5 ª 2016 John Wiley & Sons Ltd D. H. Hembry and B. Balukjian
(a) (b) (c)
(d) (e) (f)
Figure 4 Vegetation and landscapes of the Society Islands. (a) Maupiti (4.2–4.6 Ma, 380 m elev., 8 km2) is the oldest high island in the archipelago. (b) Mt. Ohiri (590 m elev.), the highest mountain on Tahaa (2.6–3.3 Ma) (c) Montane scrub dominated by Gahnia (Poaceae) and Pandanus (Pandanaceae) on Te Mehani Rahi Plateau, Raiatea (2.4–2.8 Ma) (d) View of the highly dissected interior of Tahiti Nui (0.3–1.25 Ma), Tahiti from the summit of Mt. Aorai (2066 m elev.) (e) Cloud forest dominated by Weinmannia (Cunoniaceae) and Cyathea (Cyatheaceae) on Mt. Marau, Tahiti Nui, Tahiti. (f) Mehetia (0.03 Ma-present, 435 m elev., 2.3 km2) is the youngest subaerial and only geologically active, island in the Societies. the small trees Fuchsia (of New Zealand origin; Berry et al., monophyly (four; Table 2). Some of polyphyletic/para- 2004) and Polyscias (sister to a clade of apparently Melane- phyletic groups are best interpreted as repeated indepen- sian taxa; Eibel et al., 2001); the tree snail Succinea pudorina dent colonizations of the Societies from elsewhere: these (apparently of Hawaiian origin; Holland & Cowie, 2009), include the forest herbs Peperomia (Piperaceae; Bradley, and the beetle Bembidion (sister to Australian taxa; Maddison 2003), the understorey shrubs Cyrtandra (Gesneriaceae; & Liebherr, 2013). The small herb Peperomia fosbergii (possi- Clark et al., 2009), Psychotria (Rubiaceae; Barrab e et al., bly related to Hawaiian congeners) may be an additional 2012, 2014) and Melicope (Rutaceae; Meyer et al., 2012), example (Bradley, 2003). Whether these lineages directly col- succineid snails (Holland & Cowie, 2009), Tetragnatha spi- onized Tahiti from elsewhere and were never present on ders (Gillespie, 2002; Gillespie et al., 2008; Casquet et al., other adjacent islands, or have since been extirpated on these 2015), Epicephala moths (leafflower moths; Hembry et al., other islands, is unclear. 2013a) and kingfishers (the Chattering Kingfisher Todiram- All these results suggest that the Societies biota shows the phus tutus and the Society Kingfisher T. veneratus; Ander- most phylogenetic affinities with the geographically nearest sen et al., 2015b). Peperomia, Cyrtandra, Melicope, island groups within south-eastern Polynesia (Cooks, Australs Epicephala, Tetragnatha and Succineidae all show evidence and Tuamotus) as well as the largest (by land area) oceanic of the repeated colonization of the same island (Table 2). island groups on the Pacific Plate (Marquesas, Hawaii and Other groups are more likely to represent radiations within Samoa), as would be predicted by island biogeography theory the Societies that then colonized other archipelagos; the (MacArthur & Wilson, 1967). Generally, nearly all of these strongest example of this are Partula snails, in which the Societies taxa are ultimately of Asian/Australasian origin, in single endemic species from Rarotonga (Cook Islands) is contrast with the pattern in Hawaii, where many lineages are nested within the species-rich Societies radiation (Lee et al., of New World origin (Cowie & Holland, 2008; Baldwin & 2014). Given that the Societies are larger in total land area Wagner, 2010; but see Garb & Gillespie, 2006). than any of their adjacent archipelagos, and that they are older than some surrounding islands (e.g. Rarotonga and re-uplifted islands such as Rurutu, Rimatara and some of POLYPHYLY OF SOCIETIES TAXA (MULTIPLE the north-western Tuamotus and southern Cooks), their COLONIZATIONS OR SOCIETIES AS A SOURCE role as a source of propagules for adjacent archipelagos is AREA) to be expected. Other examples of polyphyletic groups are More genera (at least thirteen) show evidence of polyphyly more ambiguous with respect to the history of colonization or paraphyly in the Society Islands than strongly supported of the Societies.
6 Journal of Biogeography ª 2016 John Wiley & Sons Ltd Society Islands phylogeography
(a) (b) (c) (d)
(e) (f) (g) (h)
(i) (j) (k) (l)
Figure 5 Examples of Societies taxa for which phylogenetic or phylogeographical data are available. (a) Astelia nadeaudii (Asteliaceae) represents a colonization of the Societies from New Zealand (photo: Moorea). (b) Santalum insulare (Santalaceae) is one plant taxon showing differentiation between the Leeward and Windward Islands (photo: Moorea). (c) Glochidion (Phyllanthaceae: Phyllanthus s. l.) is the most extensively sampled large endemic plant radiation (14 spp.) in the Societies, showing close affinities with congeners elsewhere in south-eastern Polynesia and Samoa (photo: P. emarginatus/syn. G. emarginatum, Raiatea). (d) Metrosideros collina (Myrtaceae) in the Societies is most closely related to conspecifics in the Australs and southern Cooks (photo: Moorea). (e) Peperomia (Piperaceae) likely colonized the Society Islands two or three times independently (photo: Tahiti). (f) Sclerotheca (Campanulaceae) is an endemic genus to south-eastern Polynesia, most closely related to the other south-eastern-Polynesian-endemic lobeliad genus Apetahia (photo: S. forsteri, Moorea). (g) Societies Samoana snails are closely related to congeners from the Australs and Marquesas. (h) Partula snails are one of the most species-rich endemic Societies radiations and one of the few groups showing within-island diversification (photo: Moorea). (i) Pseudoloxops plant bugs show both within- and between-island diversification and transitions from angiosperm to fern feeding (P. sp. nov., Tahiti). (j) Rhyncogonus weevils have diversified extensively through isolation on different islands and massifs within islands (photo: Huahine). (k) Todiramphus kingfishers have likely colonized the Windward and Leeward Islands independently (Society Kingfisher, T. veneratus, Tahiti, photo E. Spotswood). (l) Ptilinopus purpuratus (Grey-green Fruit Dove) are polyphyletic in the Societies, forming a clade with P. rarotongensis from the Cooks (photo L. Stevenson).
In contrast, only a few plant and animal taxa examined eties, suggesting that most of the larger endemic ‘radiations’ show strongly supported monophyly within the Societies. in the Society Islands may be polyphyletic. These are the sandalwood Santalum insulare (Santalaceae; Butaud et al., 2005; Harbaugh & Baldwin, 2007), the forest BETWEEN-ISLAND PHYLOGEOGRAPHICAL herbs Ophiorrhiza (Rubiaceae; Nakamura et al., unpublished BARRIERS IN THE SOCIETIES data), Misumenops crab spiders (Garb & Gillespie, 2009) and Coridromius plant bugs (Tatarnic & Cassis, 2013). Additional By far, the most common phylogeographical division seen in taxon sampling outside the Societies might render either Societies taxa is between the Windward and Leeward Society Ophiorrhiza or Coridromius polyphyletic. Except for Ophior- Islands (Fig. 3b). This represents the largest interisland dis- rhiza, none of these taxa are particularly diverse in the Soci- tance in the Societies (150 km between Huahine and
Journal of Biogeography 7 ª 2016 John Wiley & Sons Ltd D. H. Hembry and B. Balukjian
(a) all taxa (b) comprehensively sampled taxa 1−3 taxa 4−6 taxa 7−9 taxa 10−13 taxa 1−3 taxa 4−6 taxa 7−9 taxa
20 20
0 0
−20 −20
−40 −40
140 160 180 −160 −140 −120 140 160 180 −160 −140 −120
(c) angiosperms (d) animals 1−3 taxa 4−6 taxa 1−3 taxa 4−6 taxa 7−9 taxa
20 20
0 0
−20 −20
−40 −40
140 160 180 −160 −140 −120 140 160 180 −160 −140 −120
Figure 6 Maps representing the distributions of closely related taxa to Societies-endemic lineages. Lines between the Societies and other archipelagos/regions are not meant to imply directionality. Line segment thicknesses and colours correspond to numbers of taxa showing particular sister-group relationships. A Societies taxon may be closely related to taxa in multiple other regions in cases where phylogenetic reconstructions are ambiguous (e.g. polytomies). Regions to which lines point are as follows: Cook Islands, Marquesas Islands, Tuamotu Islands, Austral Islands, Gambier Islands, Pitcairn Islands, Hawaii, Samoa, Tonga, Fiji, Wallis and Futuna, Caroline Islands (Micronesia), New Caledonia, Australia and New Zealand. (a) All taxa. (b) Studies in which sampling of extant taxa inside and outside the Societies is either ‘extensive’ or ‘comprehensive’. (c) Angiosperms only. (d) Animals only.
Table 2 Taxa showing evidence for monophyly or polyphyly/paraphyly of particular genera in the Society Islands.
Co-occurrence on Sampling within Sampling outside Taxon Pattern same island Societies Societies
Peperomia (Piperaceae) Polyphyly Yes (Tahiti) Comprehensive Partial Cyrtandra (Gesneriaceae) Polyphyly Yes (Huahine) Limited Partial Psychotria (Rubiaceae) Polyphyly Unknown Limited Partial Ixora (Rubiaceae) Paraphyly N/A Partial Partial Melicope (Rutaceae) Polyphyly Yes (Tahiti) Extensive Partial Succineidae Polyphyly Yes (Tahiti) Unclear Extensive Partula (Partulidae) Paraphyly N/A Extensive Extensive Tetragnatha (Tetragnathidae) Polyphyly Yes (Tahiti, Moorea) Extensive Partial Epicephala (Gracillariidae) Polyphyly Yes (Tahiti, Moorea, Comprehensive Partial Huahine, Raiatea) Rhyncogonus (Curculionidae) Paraphyly N/A Comprehensive Comprehensive Acrocephalus (Acrocephalidae) Paraphyly N/A Comprehensive Comprehensive Todiramphus (Alcedinidae) Polyphyly No Extensive Comprehensive Ptilinopus purpuratus (Columbidae) Paraphyly N/A Extensive Comprehensive Santalum insulare (Santalaceae) Monophyly N/A Comprehensive Comprehensive Ophiorrhiza (Rubiaceae) Monophyly N/A Comprehensive Partial Misumenops (Thomisidae) Monophyly N/A Comprehensive Unclear Coridromius (Miridae) Monophyly N/A Unclear Unclear
Moorea), and consequently an important role for allopatry spiders (Garb & Gillespie, 2006, 2009), the two older Epi- in the diversification of the Societies biota. This pattern is cephala lineages (Hembry et al., 2013a), Pseudoloxops plant seen in a number of animal taxa, including Misumenops crab bugs (Balukjian, 2013), Rhyncogonus weevils (Claridge, 2006),
8 Journal of Biogeography ª 2016 John Wiley & Sons Ltd Society Islands phylogeography
Todiramphus kingfishers (Andersen et al., 2015b), the sandal- lineages are more widely reported. The second would imply wood Santalum insulare (Butaud et al., 2005) and probably that a substantial part of the Societies biota is much younger also the Grey-green Fruit Dove Ptilinopus purpuratus (Cibois than the archipelago itself (see data below). Finally, many et al., 2014). Acrocephalus reed warblers may also be consis- groups that are likely to show phylogeographical structure tent with this pattern as well (Cibois et al., 2008, 2011). have yet to be examined at all using molecular methods (see There are, however, exceptions: Huahine Partula are sister to Future Directions). the rest of the radiation (Lee et al., 2014). A few animal taxa (Tetragnatha, Pseudoloxops, Acro- WITHIN-ISLAND PHYLOGEOGRAPHICAL cephalus, perhaps Ptilinopus purpuratus) show evidence for BARRIERS distinct clades or sister-species on Tahiti and Moorea (Cibois et al., 2008, 2011, 2014; Gillespie et al., 2008; Balukjian, Several invertebrate radiations in the Society Islands show 2013), although other animals do not show this divergence evidence for diversification within islands. Limited gene and (Misumenops: Garb & Gillespie, 2009; Epicephala: Hembry taxon sampling suggests possible divergences between the et al., manuscript; Todiramphus veneratus: Andersen et al., two major volcanoes of Tahiti (Tahiti Nui and Taiarapu) in 2015b). Partula have multiple clades endemic to Tahiti and succineid snails (Holland & Cowie, 2009), the snail Samoana Moorea respectively, as well as clades containing taxa from burchi (Lee et al., 2009) and the spider Tetragnatha rava both islands (Lee et al., 2014), and one sister-species rela- (Gillespie et al., 2008). The radiations of Partula snails, Pseu- tionship between a Tahiti-endemic and a Moorea-endemic doloxops plant bugs, Rhyncogonus weevils and Simulium species is known in Simulium (Joy & Conn, 2001). Although blackflies show evidence for both within-island speciation (as molecular phylogenetic data are not available, multiple pairs well as between-island speciation: above). Partula contains a of presumed sister-species (based on morphology) in Mecy- number of mitochondrial clades containing multiple species clothorax ground beetles distributed on the western part of all endemic to the same island (seen on Raiatea, Huahine, Tahiti Nui and Mt. Tohiea on Moorea suggest a role for Moorea and Tahiti), suggesting within-island diversification repeated independent dispersal and between-island speciation in both the Leewards and Windwards (Lee et al., 2008, in this large insect radiation (Liebherr, 2012). 2014). Sister-species relationships in Pseudoloxops plant bugs The only groups which show evidence for inter-island show evidence of diversification within islands in six cases divergences or single-island endemic clades within the Lee- compared to between islands in two cases. The former ward Islands are Partula, Pseudoloxops and Rhyncogonus, all include potential cases of diversification within Tahiti, even of which are highly species-rich in the archipelago (Claridge, potentially within single massifs (e.g. Aorai; Balukjian, 2013). 2006; Balukjian, 2013; Lee et al., 2014). Finally, many plant Rhyncogonus weevils show diversification within Tahiti, with taxa examined (Glochidion, Ixora, Melicope tahitensis+lucida) speciation driven by isolation on different mountains/massifs show no phylogeographical structure within the archipelago evidenced by two allopatrically distributed species pairs (Mouly et al., 2009; Meyer et al., 2012; Hembry et al., (Claridge, 2006). Both these pairs consist of allopatrically 2013a), although this is in part likely due to the markers distributed sister-species, one endemic to the western Tahi- used (but see Wikstroemia; Meyer et al., 2012). The only tian massif comprised of the mountains Marau, Aorai, Pito group that shows a pattern consistent with any form of a Hiti and Pihaiateta, and one endemic to the eastern Tahitian ‘progression rule’ (Fig. 3a) is one clade of Rhyncogonus, massif of Mt. Mauru (at eastern and western ends of the which may have initially diversified on Raiatea before colo- remnants of the main shield of Tahiti Nui; Hildenbrand nizing the older islands Tahaa and Bora Bora, as well as the et al., 2004). Phylogenetic patterns are consistent with specia- younger islands Huahine, Moorea and Tahiti. tion within Raiatea and within Bora Bora in Rhyncogonus as The fact that by far the most widely seen phylogeographi- well. Diversification within Tahiti is also likely in Simulium cal barrier is the one between the Windwards and Leewards blackflies – most of the 25 species in this endemic radiation suggests two possible historical biogeographical explanations, are endemic to Tahiti, and several sister-species pairs within which are not mutually exclusive. First, the interisland dis- Tahiti are seen the phylogeny (Joy & Conn, 2001; Joy et al., tances within the Windwards and within the Leewards (at 2007). Finally, many pairs of presumed sister-species based present, 5–52 km) might not be great enough to restrict gene on morphology in the spectacular radiation of Mecyclothorax flow in many of these taxa. With the exception of Raiatea ground beetles (101 spp. on Tahiti, 7 spp. on Moorea) are and Tahaa, these islands were not connected during recent reported from different massifs or peaks within Tahiti Nui glacial maxima. The other possibility is that colonization of (Liebherr, 2013). Localized distributions of some Nabis dam- the Societies by some of these lineages has been so recent sel bugs (Heteroptera: Nabidae) species endemic to Tahiti that only the greatest inter-island separation has been effec- suggest the possibility of within-island speciation in this tive as a barrier driving phylogeographical differentiation. well-studied endemic radiation (Polhemus, 2010). Although these hypotheses are difficult to distinguish given These studies above indicate that isolation on the two available data, the former suggests that the diversification of main volcanoes of Tahiti (Tahiti Nui and Taiarapu) may the Societies biota operates differently than in other well-stu- promote population divergence (and perhaps incipient speci- died oceanic archipelagos, in which single-island-endemic ation) in some snails and spiders. There is also good
Journal of Biogeography 9 ª 2016 John Wiley & Sons Ltd D. H. Hembry and B. Balukjian 8 crown ages stem ages 6 4 2 Number of clades 0
0−2 2−4 4−6 6−8 8−10 10−12 12−14 14−16 Ages (Ma)
Figure 7 Bar chart indicating estimated divergence times for Societies taxa compiled from other studies, in two-million-year bins. Studies with extremely limited extant taxon sampling or which use geological calibrations from within the Society Islands are excluded. Dark grey indicates crown ages of clades within the Societies and light grey indicates divergence times from closest known relatives outside the Societies (stem ages). Bins are inclusive of the higher value of the bin, so that a published divergence time of 2 Ma is counted in the 0–2 Ma bin rather than the 2–4 Ma bin. Estimates that span two bins (particularly older stem-age estimates) are each assigned 0.5 to each bin. Sources of error for some (but not all) of these studies include incomplete extant taxon sampling, the use of published rates rather than calibrations and reliance on mitochondrial data. See main text for details. evidence that the erosion of the main shield of Tahiti Nui (Samoana). Divergence time estimates for the split of Soci- drove speciation in some of the archipelago’s most diverse eties taxa from their nearest known relatives elsewhere (stem insect radiations (Rhyncogonus, Simulium and Mecyclothorax) ages) show more spread, although most of those are less than – primarily through the isolation of populations on different 6 Ma in age (Fig. 7). None of these studies incorporate spe- peaks and massifs. Most importantly, these results show that cies-tree-based divergence time estimation. The primary the largest islands in the archipelago (particularly Tahiti and sources of error in these studies are likely due to missing Raiatea, but also Huahine, Moorea and possibly Bora Bora) extant taxa (which is particularly likely to affect stem-age are or have been large enough in the recent geological past estimates, and estimates in arthropods), and the use of pub- to permit within-island speciation and radiation in small- lished rates rather than calibrations (e.g. Campsicnemus, bodied invertebrates. Todiramphus and Acrocephalus). Although mitochondrial estimates can be biased towards older dates, two of the three studies which rely on mitochondrial data (Samoana and HOW OLD IS THE SOCIETIES BIOTA? Acrocephalus) estimate dates < 2 Ma. Taken together, this Limited evidence for phylogeographical divergence among evidence is consistent with the hypothesis that many Soci- adjacent islands within the Windward and Leeward Society eties lineages are much younger than the current high Islands, and abundant evidence for repeated colonizations by islands. closely related lineages, suggest that much of the extant Soci- A few Societies groups show evidence that may be consis- eties biota may in fact be much younger than the archipelago tent with their ancestors colonizing the archipelago (or a itself. A corollary of this hypothesis is that over evolutionary neighbouring one) before the formation of the current high time-scales, turnover among lineages on the Society Islands islands. Two plant genera (Astelia and Fuschia) are repre- may be high (although in some cases, these lineages may be sented by single species at high elevations in the Societies extremely closely related). Do estimated divergence times of which colonized from New Zealand. Estimates of divergence Societies clades support this hypothesis? time from New Zealand relatives in both cases (6 Ma for Many phylogenetic studies of Societies taxa have incorpo- Astelia, 8 Ma for Fuschia) are much older than 4.6 Ma, and rated divergence time estimates (see Appendix S2). Excluding in the case of Fuschia, also much older than the only island groups whose estimates are calibrated using geological ages where it is presently found (Tahiti, 1.3 Ma). These taxa are of the Societies themselves (internal calibrations) or for also absent from nearby high islands in the Cooks and Aus- which taxon sampling within the Societies is extremely lim- trals (Astelia rapensis from Rapa is a separate colonization). ited, the crown ages of nearly all (8 out of 10) Societies These patterns suggest that both Astelia and Fuschia may endemic clades have been dated to ≤ 2 Ma (corresponding have been present in south-eastern Polynesia much longer to younger than the Leeward Islands but older than the than the ages of the islands where they are presently dis- Windwards; Fig. 7). These include all of the bird radiations tributed, or have closer relatives in New Zealand which are that have been dated, two plant taxa (Sclerotheca and now extinct. A third example are Rhyncogonus weevils. Raro- Santalum; Givnish et al., 2009) and one snail clade tongan and Hawaiian Rhyncogonus each nest within a para-
10 Journal of Biogeography ª 2016 John Wiley & Sons Ltd Society Islands phylogeography phyletic grade of Society Islands taxa, the crown age of which the Leeward Islands (particularly Otemanu on Bora Bora, is c. 11 Ma with a range of c.8–15 Ma (Claridge, 2006). which has never been visited by scientists, and Ohiri on These estimates rely on mitochondrial data, but if accurate, Tahaa and Toomaru on Raiatea, which have only recently they may represent multiple colonizations of the Societies been visited a few times; J.-Y. Meyer, pers. comm., 2014), from a place where Rhyncogonus is no longer present (extant and unclimbed summits on Tahiti (e.g. Tevaitoi on Tahiti Rhyncogonus lineages in the Australs are a different clade) or Nui and Ronui on Taiarapu; J.-Y. Meyer and R. Taputuarai, colonization of now awash Societies volcanoes > 4.6 Ma. The pers. comm., 2014). final, and perhaps most intriguing example, is the Polynesian 3. Molecular dating and phylogeographical patterns suggest sandpiper genus Prosobonia (Cibois et al., 2012). The single that a large component of the Societies biota might be young extant member of this genus, the Tuamotu Sandpiper relative to the age of the existing high islands (4.6 Ma). The (P. parvirostris) is closely related to a number of extinct Societies may thus be frequently colonized, but have very described and undescribed species from Tahiti, Moorea, Kiri- high turnover. This hypothesis can be tested with additional bati, the Cooks, Australs, Marquesas and Pitcairns. Diver- molecular dating studies and modelling approaches. gence between the extinct Tahitian endemic P. leucoptera 4. Many studies suggest that the Societies may function as a and Tuamotu P. parvirostris dates to only 1.7 Ma. However, ‘stepping stone’ or ‘source area’ for the biota of different phylogenetic analysis reveals that Prosobonia shares a most archipelagos within south-eastern Polynesia (and beyond). recent common ancestor with its closest living relatives Further studies with widespread sampling from diverse (other sandpipers and turnstones) 20–35 Ma. The ancestors groups may reveal an important role for this archipelago in of this lineage probably colonized the remote Pacific during eastern Pacific biogeography, particularly islands younger the Oligocene, long before the formation of any of the extant than 4.6 Ma in neighbouring archipelagos, such as Rarotonga high islands. and the uplifted northern Australs, southern Cooks and western Tuamotus. 5. The Societies offer opportunities to study interactions FUTURE DIRECTIONS between different colonizations of the archipelago by closely Although in recent years, an increasing number of investiga- related lineages (e.g. multiple colonizations by Cyrtandra, tors have focused on the Society Islands and a number of Epicephala; possibly also Peperomia, Tetragnatha). emergent patterns are seen across Societies taxa, much 6. Within-island patterns have received relatively little atten- remains unclear both about the biodiversity of this archipe- tion in the Societies, but have been found to be very interest- lago and its patterns of molecular biogeography. Here we ing in other archipelagos. suggest major gaps in our knowledge and promising phenomena for future research: CONCLUSIONS 1. Many of the most diverse groups in the Society Islands have not been studied using molecular phylogenetic or even The molecular evolution and diversification of the biota of taxonomic approaches, which constrains our ability to draw the Society Islands shows a number of general patterns across conclusions about patterns like within- and between-island taxa within the archipelago. Many Society Islands taxa show speciation, biogeographical barriers and progression rules. sister relationships with other archipelagos in south-eastern Candidate groups for future taxonomic and phylogenetic Polynesia (particularly the Cook, Austral and Marquesas work include (in plants) Myrsine (Myrsinaceae), Bidens Islands) or other tropical Pacific islands. Many plants show (Asteraceae), Ixora (Rubiaceae), Psychotria (Rubiaceae), Cyr- affinities with western Polynesia, Fiji and New Zealand, while tandra (Gesneriaceae), (in animals) Campsicnemis (Diptera: few animals do. Most genera are polyphyletic within the Dolichopodidae), Mecyclothorax (Coleoptera: Carabidae), Societies, representing either multiple independent coloniza- Cranopoeus (Coleoptera: Curculionidae), Atylana (Hemi- tions of the archipelago or dispersal from the Societies to ptera: Nogodinidae), Nabis (Hemiptera: Nabidae), Campy- other archipelagos. The straits between the Leeward and lomma (Hemiptera: Miridae), Oliarus (Hemiptera: Cixiidae) Windward Islands are an important biogeographical barrier and Lallemandana (Hemiptera: Cercopidae). Some major in many animal groups examined. Very few taxa examined insect radiations are likely unrecognized; based on their show strong evidence for phylogeographical differentiation diversity elsewhere (e.g. Rapa), Miocalles (Coleoptera: Cur- among islands within the Leeward or Windward groups; the culionidae) and Dichelopa (Lepidoptera: Totricidae) are likely few exceptions are the most species-rich invertebrate radia- to yield interesting patterns (Clarke, 1971; Paulay, 1985). tions, which have diversified both among and within islands. 2. Similarly, the biodiversity of some important places in Finally, there is no strong evidence for a progression rule in the Societies has not been sampled, constraining our ability the diversification of Societies radiations; only one taxon to test certain hypotheses. Many of these locations are logis- may be consistent with it. tically difficult to access and in some cases have never been Two major caveats apply to these conclusions. Many stud- visited by scientists, requiring the use of helicopters or dedi- ies which include Societies taxa sample a small fraction of cated teams with extensive experience under mountain con- the diversity within the archipelago, and only a few studies ditions. Candidate locations include the highest summits of (focussed on low-diversity bird and plant groups) sample
Journal of Biogeography 11 ª 2016 John Wiley & Sons Ltd D. H. Hembry and B. Balukjian extant diversity comprehensively throughout the Pacific. Second, these findings also have important implications for Additionally, these studies do not account for human- other hotspot archipelagos in the Pacific whose biogeography mediated extinction, either following Polynesian colonization is less well-known. In terms of size, spatial arrangement and or European colonialism. In some cases, the extent of diver- topographic complexity the Societies are more similar to many sity loss remains unclear: a few sediment cores near sea level other archipelagos – particularly the Marquesas, Cook-Austral have revealed previously unknown native insect diversity on and Samoan islands – than to Hawaii. Conversely, in terms of Moorea (Kahn et al., 2015b), and only one site (on Hua- their location in close proximity to the southern Cook, north- hine) is known for sub-fossil birds in the whole archipelago ern Austral and Tuamotu archipelagos, the Societies are much (Steadman & Pahlavan, 1992). Better sampling of extant taxa less isolated than are the Marquesas and Hawaiian islands, or should, at least, further refine these preliminary conclusions, Rapa. Future research will reveal whether the diversification particularly for plants. and assembly of the biotas of other Pacific hotspot archipela- Interestingly, the common patterns seen in Societies phy- gos are more similar to the Societies or Hawaiian models. logeography are largely different from those that would be predicted from past phylogeographical work in Hawaii ACKNOWLEDGEMENTS (Wagner & Funk, 1995; Roderick & Gillespie, 1998; Cowie & Holland, 2008; Baldwin & Wagner, 2010). Many endemic We thank Bruce Baldwin, Michael Balke, David Clague, radiations in Hawaii are monophyletic, resulting from single Jean-Yves Meyer, Dan Polhemus, Erica Newman and Nik colonizations. Hawaii is also generally not argued to be an Tatarnic for discussion, Erica Spotswood and Laura Steven- important source area for other islands or biogeographical son for the bird photos, Erica Newman, Jimmy O’Donnell regions (although exceptions to this pattern have been and Morgan Tingley for assistance with figures, Bruce Bald- recently argued: Harbaugh & Baldwin, 2007; O’Grady & win, Elin Claridge, Darko Cotoras, Rosemary Gillespie, Kari DeSalle, 2008; Harbaugh et al., 2009). Hawaii does not show Goodman, Jun Ying Lim, Jean-Yves Meyer and three anony- a single, widespread phylogeographical barrier between two mous referees for comments on an earlier version of this subsets of islands in the same manner as the Leeward/Wind- manuscript, and many other people for their assistance and ward barrier seen in the Societies; instead, it more often friendship in the field while these ideas were originally being shows a weak form of the progression rule in which early- formulated. DHH was supported by NSF grant OISE- diverging (‘basal’) lineages are found on older islands. Adap- 1159509 and also thanks Chicken and Mo’o for their com- tive radiation, and diversification within- and between panionship at Gump Station. This is contribution number islands, is more pronounced in the biota of Hawaii (and of 215 of the University of California, Berkeley’s Gump South other archipelagos such as the Gal apagos). Many of these dif- Pacific Research Station. ferences may be ascribed to the smaller size, lower elevation, ephemerality and reduced isolation of the islands in the Soci- REFERENCES eties both to each other and to other oceanic archipelagos (Keast, 1996; Hembry et al., 2013b). Andersen, M.J., Hosner, P.A., Filardi, C.E. & Moyle, R.G. There are two major implications of these patterns. First, (2015a) Phylogeny of the monarch flycatchers reveals the evolution of the biota of the Society Islands differs from extensive paraphyly and novel relationships within a major that not just of Hawaii and several phylogeographical studies Australo-Pacific radiation. Molecular Phylogenetics and from other archipelagos, but from the basic observations Evolution, 83, 118–136. underlying the general dynamic (Whittaker et al., 2008) and Andersen, M.J., Shult, H.T., Cibois, A., Thibault, J.-C., overshoot (Gillespie & Baldwin, 2009) models for the evolu- Filardi, C.E. & Moyle, R.G. (2015b) Rapid diversification tion of oceanic island biotas. These patterns suggest that the and secondary sympatry in Australo-Pacific kingfishers Societies may instead be an archipelago which is frequently (Aves: Alcedinidae: Todiramphus). Royal Society Open colonized from the outside, and has high turnover of clades Science, 2, 140375. arising from these colonizing lineages. In some ways, the Baldwin, B.G. & Wagner, W.L. (2010) Hawaiian angiosperm Societies more resemble elements of the taxon cycle and radiations of North American orgin. Annals of Botany, supertramp hypotheses articulated by Wilson (1961) and 105, 849–879. Diamond (1974) for islands further west in the Pacific. Even Balke, M., Ribera, I., Hendrich, L., Miller, M.A., Sagata, K., if some of the un-investigated, species-rich radiations in the Posman, A., Vogler, A.P. & Meier, R. (2009) New Guinea Societies prove to have diversified in parallel with the forma- highland origin of a widespread arthropod supertramp. tion of the archipelago, such a finding would not change the Proceedings of the Royal Society B: Biological Sciences, 276, overall pattern reported here. Our conclusions do not mean 2359–2367. that the general dynamic or overshoot models are wrong or Balukjian, B.J. (2013) Myriad mirids: the spectacular radiation not useful for the archipelagos on which they are based, but of Pseudoloxops plant bugs (Hemiptera: Miridae) in French simply that they may be of limited applicability for the Soci- Polynesia (and the kids that love them!). PhD Thesis, ety Islands. University of California, Berkeley.
12 Journal of Biogeography ª 2016 John Wiley & Sons Ltd Society Islands phylogeography
Barrab e, L., Buerki, S., Mouly, A., Davis, A.P., Munzinger, J. Polynesian sandpipers Aechmorhynchus parvirostris and & Maggia, L. (2012) Delimitation of the genus Margaritop- Prosobonia leucoptera. Ibis, 154, 756–767. sis (Rubiaceae) in the Asian, Australasian, and Pacific Cibois, A., Thibault, J.-C., Bonillo, C., Filardi, C.E., Watling, region, based on molecular phylogenetic inference and D. & Pasquet, E. (2014) Phylogeny and biogeography of morphology. Taxon, 61, 1251–1268. the fruit doves (Aves: Columbidae). Molecular Phylogenet- Barrab e, L., Maggia, L., Pillon, Y., Rigault, F., Mouly, A., ics and Evolution, 70, 442–453. Davis, A.P. & Buerki, S. (2014) New Caledonian lineages Claridge, E.M. (2006) The systematics and dispersal of Rhynco- of Psychotria (Rubiaceae) reveal different evolutionary his- gonus (Entiminae: Curculionidae: Coleoptera) in the central tories and the largest documented plant radiation for the Pacific. PhD Thesis, University of California, Berkeley. archipelago. Molecular Phylogenetics and Evolution, 71,15– Clark, J.R., Wagner, W.L. & Roalson, E.H. (2009) Patterns of 35. diversification and ancestral range reconstruction in the Berry, P.E., Hahn, W.J., Sytsma, K.J., Hall, J.C. & Mast, A. southeast Asian-Pacific angiosperm lineage Cyrtandra (2004) Phylogenetic relationships and biogeography of (Gesneriaceae). Molecular Phylogenetics and Evolution, 53, Fuschia (Onagraceae) based on noncoding nuclear and 982–994. chloroplast DNA data. American Journal of Botany, 91, Clarke, J.F.G. (1971) The Lepidoptera of Rapa Island. Smith- 601–614. sonian Contributions to Zoology, 56,1–282. Birch, J.L. & Keeley, S.C. (2013) Dispersal pathways across Clouard, V. & Bonneville, A. (2005) Ages of seamounts, the Pacific: the historical biogeography of Astelia s. l. islands, and plateaus on the Pacific plate. Plates, plumes, (Asteliaceae, Asparagales). Journal of Biogeography, 40, and paradigms (ed. by GR Foulger, JH Natland, DC Pres- 1914–1927. nall and DL Anderson). Geological Society of America Spe- Blais, S., Guille, G., Guillou, H., Chauvel, C., Maury, R.C., cial Paper, 388,71–90. Pernet, G. & Cotton, J. (2002) The island of Maupiti: the Cowie, R.H. & Holland, B.S. (2008) Molecular biogeography oldest emergent volcano in the Society hot spot chain and diversification of the endemic terrestrial fauna of the (French Polynesia). Bulletin de la Soci et eg eologique de Hawaiian Islands. Philosophical Transactions of the Royal France, 173,45–55. Society B: Biological Sciences, 363, 3363–3376. Bradley, U. (2003) Biogeography and speciation of the genus Coyne, J.A. & Orr, H.A. (2004) Speciation. Sinauer Associ- Peperomia Ruiz & Pav on in Eastern Polynesia. PhD Thesis, ates, Sunderland, Massachusetts. Trinity College, University of Dublin. Craig, D.A. & Curie, D.C. (1999) Phylogeny of the central- Butaud, J.-F., Rives, F., Verhaegen, D. & Bouvet, J.-M. western Pacific subgenus Inseliellum (Diptera: Simuliidae). (2005) Phylogeography of Eastern Polynesian sandalwood Canadian Journal of Zoology, 77, 610–623. (Santalum insulare), an endangered tree species from the Darwin, C. (1839) Journal of researches into the geology and Pacific: a study based on chloroplast microsatellites. Jour- natural history of the various countries visited by H. M. S. nal of Biogeography, 32, 1763–1774. Beagle. Colburn, London. Cantley, J.T., Swenson, N.G., Markey, A. & Keeley, S.C. Darwin, C. (1859) On the origin of species by means of natu- (2014) Biogeographic insights on Pacific Coprosma ral selection. John Murray, London. (Rubiaceae) indicate two colonizations to the Hawaiian Diamond, J.M. (1974) Colonization of exploded volcanic Islands. Botanical Journal of the Linnean Society, 174, islands by birds: the supertramp strategy. Science, 184, 412–424. 803–806. Carlquist, S. (1974) Island biology. Columbia University Diraison, C., Bellon, H., Leotot, C., Brousse, R. & Barsczus, Press, New York, NY. H.G. (1991) L’alignement de la Soci et e (Polyn esie Casquet, J., Bourgeois, Y.X.C., Cruaud, C., Gavory, F., Gille- francßaise): volcanologie, g eochronologie, proposition d’un spie, R.G. & Th ebaud, C. (2015) Community assembly on mod ele de point chaud. Bulletin de la Soci et eg eologique de remote islands: a comparison of Hawaiian and Mascarene France, 162, 479–496. spiders. Journal of Biogeography, 42,39–50. Duncan, R.A. & McDougall, I. (1976) Linear volcanism in Cibois, A., Thibault, J.-C. & Pasquet, E. (2004) Biogeography French Polynesia. Journal of Volcanology and Geothermal of eastern Polynesian monarchs (Pomarea): an endemic Research, 1, 197–227. genus close to extinction. The Condor, 106, 837–851. Eibel, J.M., Plunkett, G.M. & Lowry, P.P., II (2001) Evolu- Cibois, A., Thibault, J.-C. & Pasquet, E. (2008) Systematics tion of Polyscias sect. Tieghemopanax (Araliaceae) based of the extinct reed-warblers Acrocephalus of the Society on nuclear and chloroplast DNA sequence data. Adanso- Islands of eastern Polynesia. Ibis, 150, 365–376. nia, 23,23–48. Cibois, A., Beadell, J.S., Graves, G.R., Pasquet, E., Slikas, B., Evenhuis, N.L. (2013) The Campsicnemus popeye species Sonsthagen, S.A., Thibault, J.-C. & Fleischer, R.C. (2011) group (Diptera: Dolichopodidae) from French Polynesia. Charting the course of reed-warblers across the Pacific Zootaxa, 3694, 271–279. islands. Journal of Biogeography, 38, 1963–1975. Fisher, R.N. (1997) Dispersal and evolution of the Pacific Cibois, A., Dekker, R.W.R.J., Pasquet, E. & Thibault, J.-C. Basin gekkonid lizards Gehyra oceanica and Gehyra muti- (2012) New insights into the systematics of the enigmatic lata. Evolution, 51, 906–921.
Journal of Biogeography 13 ª 2016 John Wiley & Sons Ltd D. H. Hembry and B. Balukjian
Florence, J. (1997) Flore de la Polyn esie francßaise, Vol. 1. Edi- dispersal in the Pacific: an example from the plant genus tions de l’ORSTOM, Paris, France. Melicope (Rutaceae). Journal of Biogeography, 36, 230–241. Garb, J.E. & Gillespie, R.G. (2006) Island hopping across the Hembry, D.H., Kawakita, A., Gurr, N.E., Schmaedick, M.A., central Pacific: mitochondrial DNA detects sequential Baldwin, B.G. & Gillespie, R.G. (2013a) Non-congruent colonization of the Austral Islands by crab spiders (Ara- colonizations and diversification in a coevolving pollina- neae: Thomisidae). Journal of Biogeography, 33, 201–220. tion mutualism on oceanic islands. Proceedings of the Royal Garb, J.E. & Gillespie, R.G. (2009) Diversity despite dispersal: Society B: Biological Sciences, 280, 20130361. colonization history and phylogeography of Hawaiian crab Hembry, D.H., Okamoto, T., McCormack, G. & Gillespie, spiders inferred from multilocus genetic data. Molecular R.G. (2013b) Phytophagous insect community assembly Ecology, 18, 1746–1764. through niche conservatism on oceanic islands. Journal of Gemmill, C.E.C., Allan, G.J., Wagner, W.L. & Zimmer, E.A. Biogeography, 40, 225–235. (2002) Evolution of insular Pacific Pittosporum (Pittospo- Hildenbrand, A., Gillot, P.-Y. & Le Roy, I. (2004) Volcano- raceae): origin of the Hawaiian radiation. Molecular Phylo- tectonic and geochemical evolution of an oceanic intra- genetics and Evolution, 22,31–42. plate volcano: Tahiti-Nui (French Polynesia). Earth and Gillespie, R.G. (2002) Biogeography of spiders on remote Planetary Science Letters, 217, 349–365. oceanic islands of the Pacific: archipelagoes as stepping Hildenbrand, A., Gillot, P.-Y. & Bonneville, A. (2006) Off- stones? Journal of Biogeography, 29, 655–662. shore evidence for a huge landslide of the northern flank Gillespie, R.G. & Baldwin, B.G. (2009) Island biogeography of Tahiti-Nui (French Polynesia). Geochemistry Geophysics of remote archipelagos: interplay between ecological and Geosystems, 7, Q03006. doi:10.1029/2005GC001003. evolutionary processes. The theory of island biogeography Hildenbrand, A., Gillot, P.-Y. & Marlin, C. (2008) Geomor- revisited (ed. by J.B. Losos and R.E. Ricklefs), pp. 358–387. phological study of long-term erosion on a tropical vol- Princeton University Press, Princeton. canic ocean island: Tahiti-Nui (French Polynesia). Gillespie, R.G., Claridge, E.M. & Goodacre, S.L. (2008) Bio- Geomorphology, 93, 460–481. geography of the fauna of French Polynesia: diversification Holland, B.S. & Cowie, R.H. (2009) Land snail models in within and between a series of hotspot archipelagos. Philo- island biogeography: a tale of two snails. American Mala- sophical Transactions of the Royal Society B: Biological cological Bulletin, 27,59–68. Sciences, 363, 3335–3346. Howarth, D.G., Gustafsson, M.H.G., Baum, D.A. & Motley, Givnish, T.J., Millam, K.C., Mast, A.R., Paterson, T.B., T.J. (2003) Phylogenetics of the genus Scaevola (Goodeni- Theim, T.J., Hipp, A.L., Henss, J.M., Smith, J.F., Wood, aceae): implication for dispersal patterns across the Pacific K.R. & Sytsma, K.J. (2009) Origin, adaptive radiation, and Basin and colonization of the Hawaiian islands. American diversification of the Hawaiian lobeliads (Asterales: Cam- Journal of Botany, 90, 915–923. panulaceae). Proceedings of the Royal Society B: Biological Joy, D.A. & Conn, J.E. (2001) Molecular and morphological Sciences, 276, 407–416. phylogenetic analysis of an insular radiation in Pacific Goodman, K.R. & O’Grady, P. (2013) Molecular phylogeny black flies (Simulium). Systematic Biology, 50,18–38. and biogeography of the Hawaiian craneflies Dicranomyia Joy, D.A., Craig, D.A. & Conn, J.E. (2007) Genetic variation (Diptera: Limoniidae). PLoS ONE, 8, e73019. tracks ecological segregation in Pacific island black flies. Goodman, K.R., Evenhuis, N.E., Barto sov a-Sojkov a, P. & Heredity, 99, 452–459. O’Grady, P.M. (2014) Diversification in Hawaiian long- Juan, C., Emerson, B.C., Orom ı, P. & Hewitt, G.M. (2000) legged flies (Diptera: Dolichopodidae: Campsicnemus): bio- Colonization and diversification: towards a phylogeo- geographic isolation and ecological adaptation. Molecular graphic synthesis for the Canary Islands. Trends in Ecology Phylogenetics and Evolution, 81, 232–241. and Evolution, 15, 104–109. Grant, P.R. & Grant, B.R. (2008) How and why species multi- Kahn, J.G., Dotte-Sarout, E., Molle, G. & Conte, E. (2015a) ply: the adaptive radiation of Darwin’s finches. Princeton Mid- to late prehistoric landscape change, settlement his- University Press, Princeton, New Jersey. tories, and agricultural practices on Maupiti, Society Guillou, H., Maury, R.C., Blais, S., Cotton, J., Legendre, C., Islands (Central Eastern Polynesia). Journal of Island and Guille, G. & Caroff, M. (2005) Age progression along the Coastal Archaeology, 10, 363–391. Society hotspot chain (French Polynesia) based on new Kahn, J.G., Nickelsen, C., Stevenson, J., Porch, N., Dotte-Sar- unspiked K-Ar ages. Bulletin de la Soci et eg eologique de out, E., Christensen, C.C., May, L., Athens, J.S. & Kirch, France, 176, 135–150. P.V. (2015b) Mid- to late Holocene landscape change and Harbaugh, D.T. & Baldwin, B.G. (2007) Phylogeny and bio- anthropogenic transformations on Mo’orea, Society geography of the sandalwoods (Santalum, Santalaceae): Islands: a multi-proxy approach. The Holocene, 25, 333– repeated dispersals throughout the Pacific. American Jour- 347. nal of Botany, 94, 1028–1040. Keast, A. (1996) Pacific biogeography: patterns and pro- Harbaugh, D.T., Wagner, W.L., Allan, G.J. & Zimmer, E.A. cesses. The origin and evolution of Pacific island biotas, New (2009) The Hawaiian archipelago is a stepping stone for Guinea to Eastern Polynesia: patterns and processes (ed. by
14 Journal of Biogeography ª 2016 John Wiley & Sons Ltd Society Islands phylogeography
A. Keast and S.E. Miller), pp. 477–512. SPB Academic VII.D el egation a la Recherche, Papeete, French Polynesia, Publishing bv, Amsterdam. 24 pages. Available at: http://www.jymeyer.com/article- Keith, P., Vigneux, E. & Marquet, G. (2002) Atlas des pois- 22996318.html sons et des crustac es d’eau douce de Polyn esie francßaise. Meyer, J.-Y., Boisselier, M.-C., Taputuarai, R. & Florence, J. Publications scientifiques du Mus eum national d’Histoire (2012) Caract erisation taxonomique, phylog en etique et naturelle, Paris, France. ecologique des esp eces end emiques de Melicope (Rutaceae), Lee, T., Meyer, J.-Y., Burch, J.B., Pearce-Kelly, P. & O Alyxia (Apocynaceae) et Wikstroemia (Thymeleaceae) aux Foighil, D. (2008) Not completely lost: two partulid tree ^ıles Marquises: une contribution a la compr ehension de snail species persist on the highest peak of Raiatea, French l’origine et de la diversit e biologique d’un archipel de Poly- Polynesia. Oryx, 42, 615–619. n esie francßaise. Institut de recherche pour le d eveloppe- Lee, T., Burch, J.B., Coote, T., Pearce-Kelly, P., Hickman, C., ment and D el egation a la Recherche, Papeete, French Meyer, J.-Y. & O Foighil, D. (2009) Moorean tree snail Polynesia, 16 pages. Available at: http://www.li-an.fr/jyves/ survival revisited: a multi-island genealogical perspective. Meyer_et_al_2012_Rapport_Endemisme_Patrimoine_Biolo BMC Evolutionary Biology, 9, 204. gique_Marquises.pdf Lee, T., Li, J., Churchill, C.K.C. & O Foighil, D. (2014) Evo- Mouly, A., Razafimandimbison, S.G., Khodabandeh, A. & lutionary history of a vanishing radiation: isolation-depen- Bremer, B. (2009) Phylogeny and classification of the spe- dent persistence and diversification in Pacific island cies-rich pantropical showy genus Ixora (Rubiaceae-Ixor- partulid tree snails. BMC Evolutionary Biology, 14, 202. eae) with indications of geographical monophyletic units Liebherr, J.K. (2012) The first precinctive Carabidae from and hybrids. American Journal of Botany, 96, 686–706. Moorea, Society Islands: new Mecyclothorax spp. (Cara- Nishida, G. (2008) French Polynesia checklists. Available at: bidae) from the summit of Mont Tohiea. ZooKeys, 224, http://essigdb.berkeley.edu/checklists/ 37–80. O’Grady, P. & DeSalle, R. (2008) Out of Hawaii: the origin Liebherr, J.K. (2013) The Mecyclothorax beetles (Coleoptera, and biogeography of the genus Scaptomyza (Diptera: Carabidae, Moriomorphini) of Tahiti, Society Islands. Zoo- Drosophilidae). Biology Letters, 4, 195–199. Keys, 322,1–170. Parent, C.E., Caccone, A. & Petren, K. (2008) Colonization Liebherr, J.K. & Maddison, D.R. (2013) Colonization of the and diversification of Gal apagos terrestrial fauna: a phylo- Pacific by Bembidion beetles (Coleoptera: Carabidae), with genetic and biogeographical synthesis. Philosphical Trans- description of Bembidion tahitense, sp. nov. from Tahiti, actions of the Royal Society B, 363, 3347–3361. French Polynesia. Invertebrate Systematics, 27, 439–449. Paulay, G. (1985) Adaptive radiation on an isolated oceanic MacArthur, R.H. & Wilson, E.O. (1967) The theory of island island: the Cryptorhynchinae (Curculionidae) of Rapa revis- biogeography. Princeton University Press, Princeton, New ited. Biological Journal of the Linnean Society, 26,95–187. Jersey. Percy, D.M., Garver, A.M., Wagner, W.L., James, H.F., Cun- Meyer, J.-Y. (1999) Note sur la v eg etation de l’^ıle de Maupiti. ningham, C.W., Miller, S.E. & Fleischer, R.C. (2008) Pro- Fiche Technique 8, D el egation a la Recherche, Papeete, gressive island colonization and ancient origin of French Polynesia, 3 pages. Available at: http://www.li-an.fr/ Hawaiian Metrosideros (Myrtaceae). Proceedings of the jyves/Meyer_1999_Fiche_Technique_Vegetation Royal Society B: Biological Sciences, 275, 1479–1490. _Maupiti.pdf Polhemus, D.A. (2010) Eight new species of micropterous Meyer, J.-Y. (2004) Threat of invasive alien plants to native Nabidae (Heteroptera) from the Society Islands, French flora and forest vegetation of Eastern Polynesia. Pacific Polynesia, with consideration of hotspot island speciation Science, 58, 357–375. patterns. Tijdschrift Voor Entomologie, 153,53–78. Meyer, J.-Y. (2007) Rapport de mission dans l’^ıle de Mai’ao Price, J.P. & Clague, D.A. (2002) How old is the Hawaiian (Soci et e) du 24 au 29 mai 2007: inventaire pr eliminaire de la biota? Geology and phylogeny suggest recent divergence. flore et des diff erents types de v eg etation et observations sur la Proceedings of the Royal Society B: Biological Sciences, 269, faune terrestre.D el egation a la Recherche, Papeete, French 2429–2435. Polynesia, 17 pages. Available at: http://www.li-an.fr/jyves/ Roderick, G.K. & Gillespie, R.G. (1998) Speciation and phy- Meyer_2007_Rapport_mission_Maiao.pdf logeography of Hawaiian terrestrial arthropods. Molecular Meyer, J.-Y. (2010) Montane cloud forests on remote islands Ecology, 7, 519–531. of Oceania: the example of French Polynesia (south Pacific Rundell, R.J., Holland, B.S. & Cowie, R.H. (2004) Molecular Ocean). Tropical montane cloud forests: science for conserva- phylogeny and biogeography of the endemic Hawaiian tion and management (ed. by L.A. Bruijnzeel, F.N. Scatena Succineidae (Gastropoda: Pulmonata). Molecular Phyloge- and L.S. Hamilton), pp. 121–129. Cambridge University netics and Evolution, 31, 246–255. Press, Cambridge. Steadman, D.W. (2006) Extinction and biogeography of tropical Meyer, J.-Y., Fourdrigniez, M. & Taputuarai, R. (2009) Eval- Pacific birds. Chicago University Press, Chicago, Illinois. uation de la biodiversit e terrestre de l’^ıle de Me’eti’a Steadman, D.W. & Pahlavan, D.S. (1992) Extinction and bio- (archipel de la Soci et e). Contribution a la Biodiversit ede geography of birds on Huahine, Society Islands, French Polyn esie francßaise N°18. Sites Naturels d’Int er^et Ecologique Polynesia. Geoarchaeology, 7, 449–483.
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Swenson, U., Munzinger, J. & Bartish, I.V. (2007) Molecular SUPPORTING INFORMATION phylogeny of Planchonella (Sapotaceae) and eight new species from New Caledonia. Taxon, 56, 329–354. Additional Supporting Information may be found in the Tatarnic, N.J. & Cassis, G. (2013) Surviving in sympatry: online version of this article: paragenital divergence and sexual mimicry between a pair Appendix S1 Distributions of sister groups to Society of traumatically inseminating plant bugs. The American Island lineages. Naturalist, 182, 542–551. Appendix S2 Estimated divergence times for the crown Tronchet, F., Plunkett, G.M., J er emie, J. & Lowry, P.P., II ages of Societies-endemic clades and their divergences from (2005) Monophyly and major clades of Meryta (Arali- sister groups outside of the Societies. aceae). Systematic Botany, 30, 657–670. Uto, K., Yamamoto, Y., Sudo, M., Uchiumi, S., Ishizuka, O., BIOSKETCHES Kogiso, T. & Tsunakawa, H. (2007) New K-Ar ages of the Society Islands, French Polynesia, and implications for the David Hembry is a postdoctoral researcher at the Univer- Society hotspot feature. Earth, Planets and Space, 59, 879– sity of Arizona interested in the evolution of interactions, 885. particularly those between leafflower moths (Epicephala) and Wagner, W.L. & Funk, V.A. (1995) Hawaiian biogeography: leafflower plants (Phyllanthus s. l.) in the Society Islands and evolution on a hotspot archipelago. Smithsonian Institution elsewhere in the world. Press, Washington, DC. Whittaker, R.J., Triantis, K.A. & Ladle, R.J. (2008) A general Brad Balukjian is adjunct faculty at Laney College in Oak- dynamic theory of oceanic island biogeography. Journal of land, California and is interested in island biogeography and Biogeography, 35, 977–994. the taxonomy of understudied Hemiptera (which means all Wilson, E.O. (1961) The nature of the taxon cycle in the Hemiptera). Melanesian ant fauna. The American Naturalist, 95, 169– 193. Editor: Lawrence Heaney Wright, S.D., Yong, C.G., Wichman, S.R., Dawson, J.W. & Gard- ner, R.C. (2001) Stepping stones to Hawaii: a trans-equatorial pathway for Metrosideros (Myrtaceae) inferred from nrDNA (ITS+ETS). Journal of Biogeography, 28, 769–774.
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