Origins of Species Richness in the Indo‐Malay‐Philippine Biodiversity
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Journal of Biogeography (J. Biogeogr.) (2013) 40, 1638–1648 SYNTHESIS Origins of species richness in the Indo-Malay-Philippine biodiversity hotspot: evidence for the centre of overlap hypothesis Michelle R. Gaither* and Luiz A. Rocha California Academy of Sciences, Section of ABSTRACT Ichthyology, San Francisco, CA, 94118, USA The Indo-Malay-Philippine (IMP) biodiversity hotspot, bounded by the Philip- pines, the Malay Peninsula and New Guinea, is the epicentre of marine biodi- versity. Hypotheses to explain the source of the incredible number of species found there include the centre of overlap hypothesis, which proposes that in this region the distinct faunas of the Pacific and Indian Oceans overlap. Here we review the biogeographical evidence in support of this hypothesis. We examined tropical reef fish distributions, paying particular attention to sister species pairs that overlap in the IMP hotspot. We also review phylogeographi- cal studies of wide-ranging species for evidence of lineage divergence and over- lap in the IMP region. Our synthesis shows that a pattern of isolation between the Pacific and the Indian Ocean faunas is evident across a wide range of taxa. The occurrence of sister species, with one member in each ocean, indicates that the mechanism(s) of isolation has been in effect since at least the Miocene, while phylogeographical studies indicate more recent divergences in the Pleisto- cene. Divergence in isolation followed by population expansion has led to an overlap of closely related taxa or genetic lineages in the hotspot, contributing to diversity and species richness in the region. These findings are consistent with the centre of overlap hypothesis and highlight the importance of this pro- cess in generating biodiversity within the IMP. *Correspondence: Michelle R. Gaither, Keywords California Academy of Sciences, Section Biogeography, centre of accumulation, centre of origin, coral reefs, Coral of Ichthyology, 55 Music Concourse Drive, San Francisco, CA 94118, USA. Triangle, IMP hotspot, marine biodiversity, phylogenetics, phylogeography, E-mail: [email protected] species distributions. Malay-Philippine biodiversity hotspot (IMP hotspot; Fig. 1). INTRODUCTION Over 2600 species of reef fishes and 600 species of corals are The region bounded by the Philippines, the Malaysian penin- found in the IMP region (Veron et al., 2009; Allen & Erd- sula, New Guinea and northern Australia has long been rec- mann, 2012). Taxonomic diversity declines with distance ognized as a biodiversity hotspot (Stehli & Wells, 1971; from the area, both latitudinally and longitudinally: a pattern Veron, 1993; Randall, 1998; Bellwood et al., 2012; Briggs & identified in corals by Stehli & Wells (1971) and since recog- Bowen, 2013). The geographical boundaries and shape of this nized across a broad array of taxa (Paulay, 1990; Veron, hotspot differ with the viewpoint of the biogeographer, and 1995; Briggs, 1999). The generality of this pattern has led there have been various names assigned to the region. The many researchers to conclude that a common mechanism Coral Triangle defined by Veron et al. (2009) extends from may be responsible for the high biodiversity in the region. the Philippines to the Solomon Islands but does not include Several hypotheses have been proposed to explain the species the Coral Sea, while the Indo-Australian Archipelago defined richness in the IMP hotspot and these can be grouped into by Bellwood & Hughes (2001) is inclusive of the Coral Tri- four major categories: (1) centre of origin, (2) centre of angle but extends considerably north and south (Fig. 1; see accumulation, (3) centre of survival, and (4) centre of over- also Fig. 1C in Renema et al., 2008). Regardless of where the lap. Contemporary species distributions (and most recently exact boundaries are drawn there is wide agreement that this biogeographical modelling; Cowman & Bellwood, 2013) are region is the epicentre of marine biodiversity (Cowman & the most common line of evidence used to test these hypoth- Bellwood, 2013), and herein we refer to it as the Indo- eses, and, amidst the jockeying of competing models, some 1638 http://wileyonlinelibrary.com/journal/jbi ª 2013 Blackwell Publishing Ltd doi:10.1111/jbi.12126 Evidence for the centre of overlap hypothesis IMP hotspot is due in part to the overlap of distinct faunas from the Pacific and Indian Oceans (Briggs, 1974; Wood- Indo-Polynesian land, 1983). Under both the centre of accumulation and the centre of overlap hypothesis, speciation occurs in locations outside the hotspot, with subsequent dispersal into the IMP region. The difference between these two hypotheses lies in West Indian the mechanism driving divergence and the resulting distribu- Ocean tion of sister taxa. The centre of overlap hypothesis is based on the premise that the isolating mechanism is the shallow Figure 1 Map of the Indo-Pacific region showing Indo- Sunda and Sahul shelves of Indonesia, Malaysia and North- Polynesian (grey) and West Indian Ocean (blue) biogeographical ern Australia, known as the Indo-Pacific Barrier (IPB; provinces (modified from Briggs & Bowen, 2012). Boundaries Fig. 2). Under this hypothesis, the faunas of the Pacific and are drawn to outline major regions of coral reef habitat (for Indian Oceans gained distinction during historical low sea- detailed distributions visit http://www.google.com/gadgets/ level stands when dispersal was restricted between ocean directory?synd=earth&id=696770371738/). Variations in the basins. Following sea-level rise, the geographical ranges of boundaries of the west Indo-Pacific biodiversity hotspot are shown: dashed line, the Coral Triangle (Veron et al., 2009); sister taxa formerly separated by the IPB expanded and even- solid black line, the Indo-Malay-Philippine (IMP) biodiversity tually came to overlap in the IMP hotspot. Under the centre hotspot (Carpenter & Springer, 2005), which is nearly identical of accumulation hypothesis, speciation is also thought to to the East Indies Triangle (Briggs, 2003) and the Indo-Malayan occur in peripheral locations but no specific mechanism is Triangle (Donaldson, 1986); solid red line, Indo-Australian implicated; sister taxa can reside anywhere in the range, and Archipelago (Bellwood & Hughes, 2001; Renema et al., 2008). the overlap of closely related taxa at the IMP region is not For the purpose of this study we define the hotspot using the required. IMP boundary of Carpenter & Springer (2005). The arrow indicates the Cocos-Keeling Islands in the eastern Indian Ocean. The literature is replete with examples that support one hypothesis over another. Efforts to compile the evidence have have acquired vocal proponents while others receive compar- largely sought to uncover the prevailing mechanism responsi- atively little consideration. ble for the species richness of the IMP hotspot but have not First proposed by Ekman (1953), the hypothesis that has elevated any single hypothesis (Connolly et al., 2003; Mora received the most attention is that of the centre of origin. et al., 2003; Halas & Winterbottom, 2009). Emerging from Ekman (1953) and others who have followed (Briggs, 1999, decades of debate is a growing recognition that the compet- 2003) suggest that the high number of species in the IMP ing hypotheses are not mutually exclusive but in fact are hotspot is a product of an unusually high rate of speciation likely to be working in conjunction to create the species rich- in the region, with new species radiating from this centre of ness of the region (Bellwood & Hughes, 2001; Rocha et al., origin. Mechanisms invoked to explain the elevated specia- 2008; Bowen et al., 2013; Briggs & Bowen, 2013; Cowman & tion rate include the fracturing of populations as a result of Bellwood, 2013). In an effort to contribute to the growing the geological complexity of the region and eustatic sea-level understanding of the complexity of this issue we present a changes (McManus, 1985). Others have suggested that review of the evidence in support of the centre of overlap increased rates of speciation in the hotspot are driven by (C-O) hypothesis. Here, we describe the mechanism of isola- intense competition (Briggs, 2005; Bowen et al., 2013) and tion and provide evidence of the partial, and at times nearly differing selection pressures in a highly heterogeneous envi- complete, isolation of the Pacific and Indian Ocean faunas ronment (Rocha & Bowen, 2008). Several years after Ekman since at least the Miocene. proposed the centre of origin hypothesis, Ladd (1960) coun- tered with the centre of accumulation hypothesis. This model THE MECHANISM OF ISOLATION proposes speciation in peripheral locations with subsequent dispersal of novel taxa into the IMP hotspot. The long his- Woodland (1983), in his work on rabbitfishes (family Sigani- tory of the Pacific archipelagos, some of which date to the dae), noticed pairs of sister species within which one had a Cretaceous, the possibility of isolation in these peripheral distribution centred in the Pacific Ocean whilst the other’s habitats, and ocean current and wind patterns that favour was centred in the Indian Ocean, with the tails of these dispersal towards the IMP region have been suggested as ranges overlapping in the IMP region. He surmised that at mechanisms in support of this hypothesis (Ladd, 1960; Jokiel least part of the species richness in the hotspot was due to & Martinelli, 1992). Still others suggest that the habitat-rich the overlapping of distinct faunas from these two ocean IMP region is