Hembry and Balukjian 2016

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 Galapagos 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 genera) 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 archipelago. Main conclusions Much of the Societies biota does not appear to have diver- sified in parallel with the formation of the archipelago, differing from ‘progression rule’ and general dynamic models for the diversification of oceanic archipelago biotas. Rather, many Societies ‘radiations’ may have been assembled via repeated, independent colonizations, which may have entailed extensive 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, Galapagos 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 Galapagos; 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 Îles-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 Îles-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.

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