bs_bs_banner Biological Journal of the Linnean Society, 2015, 114, 212–228. With 3 figures Allopatry and overlap in a clade of snails from mangroves and mud flats in the Indo-West Pacific and Mediterranean (Gastropoda: Potamididae: Cerithideopsilla) TOMOWO OZAWA1†, WEI YIN2†, CUIZHANG FU2, MARTINE CLAREMONT3, LISA SMITH3 and DAVID G. REID3* 1Department of World Heritage, Cyber University, Nagoya Office, Ikegami-cho 2-7-1, Ikegami Jyutaku R203, Chikusa-ku, Nagoya 464-0029, Japan 2Institute of Biodiversity Science, Fudan University, Handan Road 220, Shanghai 200433, China 3Department of Life Sciences, Natural History Museum, London SW7 5BD, UK Received 2 July 2014; revised 21 August 2014; accepted for publication 21 August 2014 Cerithideopsilla is a genus of potamidid snails found in high abundance on sedimentary intertidal flats and beneath mangrove trees on continental shores in the tropical and subtropical Indo-West Pacific region and Mediterranean Sea. Taxonomic revisions have recognized four species, but recent molecular studies have hinted at a higher diversity. Here, we analyse 377 individuals sampled from across the known range and use a combination of molecular phylogenetic (mitochondrial COI and 16S rRNA, and nuclear 28S rRNA genes), statistical (generalized mixed Yule-coalescent GMYC method) and morphological (shell form) criteria to delimit 16 species. These form four species groups, corresponding with the traditionally recognized species C. alata, C. ‘djadjariensis’ (for which the valid name is C. incisa), C. cingulata and C. conica. Distribution maps were compiled using museum specimens identified by diagnostic shell characters. In combination with the molecular phylogenetic trees, these suggest an allopatric speciation mode, with diversification centred on the East Asian coastline and northern Australia, and a pronounced gap in the ‘eastern Indonesian corridor’, an area of low oceanic productivity. There is, however, frequently geographical overlap between sister species and we suggest from several sources of evidence (e.g. presence of C. conica in isolated saline lakes 900 km from the sea) that post-speciation transport by migratory birds has occurred. Nine of the 16 species occur between the Gulf of Tonkin and Hong Kong, so southern China is significant for both the evolution and conservation of Cerithideopsilla species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 212–228. ADDITIONAL KEYWORDS: allopatric speciation – GMYC – marine biogeography – southern China. INTRODUCTION (see recent reviews by Bellwood, Renema & Rosen, 2012; Bowen et al., 2013; Briggs & Bowen, 2013; Biodiversity in the shallow marine tropics shows a Cowman & Bellwood, 2013). In contrast, the evolution global maximum in the central Indo-West Pacific and biogeography of the biota of another characteris- (IWP) (Hoeksema, 2007). Documentation of this tic but far less diverse tropical biotope, the mangrove pattern, and studies of the processes that have pro- forest, have been relatively neglected (Ellison, duced and maintain it, have concentrated above all on Farnsworth & Merkt, 1999; Plaziat et al., 2001; the exceptionally species-rich biotope of the coral reef Ellison, 2002; Ricklefs, Schwarzbach & Renner, 2006). The mangrove plants, of which there are only about 70 species worldwide, typically have wide distribu- *Corresponding author. E-mail: [email protected] tions that overlap to generate the highest diversity †Joint first authors. within the Indo-Australian Archipelago (IAA) at the 212 © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 212–228 DIVERSIFICATION OF MUD-FLAT SNAILS 213 centre of the IWP (Spalding, Blasco & Field, 1997; ten to 15 species (Reid et al., 2013; Reid, 2014), and of Groombridge & Jenkins, 2002; Daru et al., 2013). The IWP Cerithideopsis from one to three species (Reid & observed global diversity gradient of mangrove- Claremont, 2014), although study of Cerithideopsis in associated animals is believed to be broadly similar, Central America has suggested a reduction in its with a peak in the central IWP, but information on diversity (Miura et al., 2010, 2012). their distributions remains limited (Ellison et al., After Cerithidea and Cerithideopsis, the third 1999; Ellison, 2002). Some members of the mangrove largest potamidid genus is Cerithideopsilla. A classi- fauna have been included in molecular phylogenetic cal study of shell morphology recognized just four analyses, either within wider systematic studies (e.g. species in the central IWP (Van Regteren Altena, Schubart et al., 2006) or in taxonomic groups that 1940), but molecular study has added another from range across adjacent habitats such as intertidal the western Indian Ocean and Mediterranean rocky (Frey & Vermeij, 2008; Frey, 2010) and sedi- (Reid et al., 2008). Furthermore, the diversity of mentary shores (Shih & Suzuki, 2008; Ozawa et al., mitochondrial lineages within several of the nominal 2009; Shih et al., 2009; Yin et al., 2009; Golding, 2012; species strongly suggests that diversity has been Chen et al., 2014; Polgar et al., 2014). However, underestimated (Kojima et al., 2006; Reid et al., 2008; studies of strictly mangrove-associated clades, from Kamimura et al., 2010). A systematic revision based which to draw inferences about phylogeography and on thorough sampling throughout the range is clearly diversification within the mangrove biotope itself, are required. The association with the mangrove environ- rare. The few studied examples include decapod crabs ment is less strict than in some other potamidid (Fratini et al., 2005; Ragionieri et al., 2009) and mol- genera. All of the nominal species of Cerithideopsilla luscs (Reid et al., 2008, 2013; Miura, Torchin & occur on intertidal mud and sandy mud substrates, Bermingham, 2010; Reid, Dyal & Williams, 2010; and several are most frequently found in the shade Miura et al., 2012; Reid & Claremont, 2014). and shelter of mangrove trees (Wells, 1985; Maki, Gastropods are a major component of the macro- Ohtaki & Tomiyama, 2002; Lozouet & Plaziat, 2008). fauna of mangrove habitats, although the number of However, the distributions of some Cerithideopsilla species is relatively low; for example only about 44 species extend beyond the northern limit of man- and 65 species of mangrove-associated molluscs (of groves in Japan and Korea (Hasegawa, 2000; Maki which most are gastropods) have been recorded in the et al., 2002; Hong, Choi & Tsutsumi, 2010) and, in the diversity focus of the central IWP, in Borneo (Ashton, Mediterranean (where no mangroves are found), Macintosh & Hogarth, 2003) and the Philippines C. conica occupies intertidal flats, shallow lagoons (Lozouet & Plaziat, 2008) respectively. Only one and even isolated saline lakes (Lozouet, 1986; Plaziat, family-level taxon shows a close association with 1993; Kowalke, 2001). In the IWP, C. cingulata occurs mangroves and warm-temperate salt marshes – the abundantly on open mud and sand flats (at densities Potamididae (review by Reid et al., 2008). This group of up to 4800 m−2), often adjacent to mangroves, but includes the large, ground-dwelling mudwhelks not necessarily sheltered by them (Vohra, 1970; Terebralia and Telescopium, which shelter beneath Balaparameswara Rao & Sukumar, 1982; Wells, mangrove trees and consume detritus, algae and (in 1985; Maki et al., 2002; Ando & Tomiyama, 2005; Terebralia palustris alone) fallen leaves. It also Willan, 2013). Densities in fish ponds may be even includes the genus Cerithidea of smaller, thin-shelled higher (up to 7000 m−2; Lantin-Olaguer & Bagarinao, species that climb on mangrove vegetation to avoid 2001). Information on mode of larval development is intense crushing predation and, perhaps, for tempera- fragmentary. Both C. cingulata and C. djadjariensis ture control. Until recently, the worldwide diversity of are reported to be planktotrophic with a length the family was estimated at 29 species, based on of larval life of about 11–20 days (Habe, 1955; taxonomic assessment of shell morphology. A molecu- Lantin-Olaguer & Bagarinao, 2001; Kimura et al., lar phylogenetic framework is now available (Reid 2002; Kojima et al., 2006), but C. conica has non- et al., 2008), defining six monophyletic genera: planktotrophic development with no planktonic stage Terebralia, Telescopium and Cerithidea in the IWP (Kowalke, 2001). only; Tympanotonos in West Africa; Cerithideopsis in The modern diversity of potamidid genera and the Americas and IWP; and Cerithideopsilla in the species is highest in the central IWP. This, combined IWP and Mediterranean. Both the fossil record and with their strict dependence on mangroves, makes the phylogenetic reconstruction of ancestral habitats them a key group for the study of diversification in suggest that the living potamidids are an adaptive this biotope. The classic explanations for the diversity radiation that has been associated with mangroves focus in the IAA have been based on various models since its origin in the Middle Eocene (Reid et al., of allopatric speciation (Bellwood et al., 2012) and, 2008). Detailed molecular and morphological analysis although there is a growing recognition of the role of of Cerithidea has increased its known diversity from parapatric ecological speciation (Bowen et al., 2013), © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 212–228 214 T. OZAWA ET AL. it is acknowledged that a degree of spatial separation Ma. It has been suggested