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Molecular Phylogenetics and Evolution 47 (2008) 680–699 www.elsevier.com/locate/ympev

Mudwhelks and : The evolutionary history of an ecological association (: )

D.G. Reid a,*, P. Dyal a, P. Lozouet b, M. Glaubrecht c, S.T. Williams a

a Department of Zoology, Natural History Museum, London SW7 5BD, United Kingdom b De´partement Syste´matique et E´ volution, Muse´um National d’Histoire Naturelle, 75005 Paris, France c Berlin Museum of Natural History, Humboldt University, D-10115 Berlin, Germany

Received 7 August 2007; accepted 7 January 2008 Available online 13 January 2008

Abstract

Most of the 29 living of Potamididae show a close association with mangroves. The trees provide the snails with shelter, pro- tection from predators, a solid substrate and sometimes food. Using sequences from three genes (nuclear 18S rRNA and 28S rRNA, mitochondrial COI) we derive a molecular phylogeny and recognize six living genera (, , , Ceri- thidea, , ). The oldest modern genera (Terebralia, Cerithideopsis) appeared in the Tethyan realm in the Mid- dle , shortly after the origin of trees. Whereas most potamidid genera are now restricted to either the Indo-West Pacific (IWP) or to the eastern Pacific plus Atlantic (EPA), sister clades of Cerithideopsis survive in both realms. Based on a reinterpretation of the record (particularly of the monotypic Tympanotonos and extinct ), and parsimonious reconstruction of ancestral hab- itats, we suggest that the living potamidids are an adaptive radiation that has always been closely associated with mangroves. The spe- cialized tree-climbing groups and Cerithideopsis were independently derived from mud-dwelling ancestors. Cerithideopsilla cingulata (a species complex in the IWP) and ‘Potamides’ conicus (in the Mediterranean and Indian ) form a single clade within the Cerithideopsilla. This refutes the hypothesis that ‘P.’ conicus is the sole relict of the Tethyan Potamides that has occurred in the Mediterranean region since the Palaeocene. Instead, the phylogeny and fossil record suggest that an ancestor of Cerithideopsilla con- ica with planktotrophic larvae dispersed from the IWP to the Mediterranean in the Middle , that its direct development evolved in the Mediterranean during the Pliocene, and that it reinvaded the during the Plio-Pleistocene. Ó 2008 Elsevier Inc. All rights reserved.

Keywords: Adaptive radiation; ; Cerithidea; Potamides; Ribosomal RNA; COI

1. Introduction son et al., 1999; Plaziat et al., 2001). This continuous distribution was disrupted by the closure of the seaways The mangrove ecosystem has an ancient history. From in the Middle East at the end of the Early Miocene (16– the record of macrofossils and pollen, the earliest appear- 18 Ma, Harzhauser et al., 2002), leading to the present sep- ance of a modern mangrove genus, the palm Nypa, has aration between the Atlantic plus Eastern Pacific (AEP), been documented in the Late , and most genera and the Indo-West Pacific (IWP) biogeographic regions of the Rhizophoraceae are known by the Early Eocene (McCoy and Heck, 1976; Ellison et al., 1999). Plaziat (about 50 Ma). By the Middle to Late Eocene most modern et al. (2001) have suggested that the separation of the man- mangrove genera showed a worldwide tropical and sub- groves of the AEP from those of the IWP began much ear- tropical distribution, centred on the Tethyan Seaway (Elli- lier, with the global cooling of the early , followed by aridity in in the early Miocene, which combined to reduce the mangroves of the Tethyan Seaway * Corresponding author. Fax: +44 20 7942 5054. to isolated stands of Avicennia alone (but see Herman and E-mail address: [email protected] (D.G. Reid). Marquet, 2007 and Doutrelepont, 2007 for a probable brief

1055-7903/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2008.01.003 D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699 681 reimmigration of Rhizophoraceae in Belgium during the and saltpans. As reviewed below, all but Cerithidea are of Middle Miocene). At the present time the species richness low taxonomic diversity and now show restricted biogeo- of mangroves in the IWP province exceeds 30 in the central graphic range, although a long Tertiary fossil record in diversity focus, whereas it is less than 10 anywhere in the the Tethys Sea has been claimed for all of them. AEP (Ellison et al., 1999; Ellison, 2002). Potamides, type genus of the family, is based on the fos- Although the Tethyan origin and vicariant history of sil P. lamarkii from the Oligocene of Europe. During the mangroves are understood in broad terms, the factors con- Miocene and Pliocene it became diverse in the European tributing to their diversity gradient are not. This has led to Tethys and Paratethys (Lozouet, 1986; Kowalke, 2001a, calls for comparative study of their associated fauna (Elli- 2003). Only a single extant species is attributed to the son, 2002). Of this fauna, the molluscs have the best fossil genus, distributed from the Mediterranean to the Red record, and are taxonomically relatively well understood. Sea, Arabia and the western Indian Ocean. Not only does The marine mangrove-associated molluscs are not very it extend into higher latitudes (40°N) than other potamid- diverse, perhaps because of the unfavourable combination ids, but unlike most of them it does not have an obligate of heavy sediment load, acidic and anoxic soil, deep shade association with the mangrove , occurring in brack- (restricting algal productivity) and intense crushing preda- ish and hypersaline lagoons, in saline lakes, at the fringes of tion. Nevertheless, at least in the IWP there exists a suite of saltpans and on mudflats adjacent to mangroves (Lozouet, mangrove-associated molluscs sufficiently characteristic 1986; Plaziat, 1993; Kowalke, 2001a). Its shell is highly var- that their occurrence in the fossil record is indicative of iable, and neither its anatomy nor relationships have been marine palaeomangrove environments (Oyama, 1950; Plaz- studied. iat, 1984, 1995). (Included as mangrove environments are Three subgenera have been recognized within Cerithidea the tropical ‘saltwort associations’ of Arthrocnemum, Sesu- sensu lato, based on the morphology of the shell and rad- vium and halophytic grasses that replace mangroves in ula, and this division corresponds with differences of habi- regions of low input of freshwater or high evaporation, tat and biogeographic distribution (Houbrick, 1984). e.g. Macnae, 1968, and share many molluscan species in Members of Cerithidea sensu stricto are restricted to the common.) The mangrove-associated molluscs of the IWP IWP, living attached to roots and trunks of mangrove include one or two species each of the gastropods Nerita trees, anchored by when dry, and sometimes migrat- and , both of which are genera otherwise found ing to the mud below to feed during low (Berry, 1972; on rocky substrates in shallow- and intertidal envi- Ohtaki et al., 2002; Vannini et al., 2006). This tree-climbing ronments. At a higher taxonomic level, the bivalve genera behaviour is apparently connected both with escape from Geloina and Enigmonia, and the gastropods Littoraria (Lit- predatory fish and crabs that enter the forest at high tide torinidae), Rhizophorimurex (Muricidae), Cassidula and and with avoidance of physiological stress (McGuiness, Ellobium (Ellobiidae) are largely restricted to mangrove 1994; Vannini et al., 2006). At least ten species can be dis- environments. However, only a single molluscan family, tinguished by their shells (Brandt, 1974; Wilson, 1993; the Potamididae (mudwhelks or mud creepers), is found Brown, 1994; Hasegawa, 2000; Ma, 2004), but there has almost exclusively among mangroves and in their suite of been no critical taxonomic revision. The subgenus Ceri- associated tidal . Potamidids are among the most thideopsis is distributed in warm temperate and tropical lat- specialized molluscan inhabitants of this ecosystem, and a itudes of the AEP. Species occur in dense populations on long evolutionary association between mudwhelks and estuarine mudflats, and most climb on or shelter beneath mangroves has been hypothesized (Glaubrecht, 1996, mangroves, saltworts and (outside the latitudinal limits of 1997, 1999). mangroves) saltmarsh grasses (Keen, 1971; Race, 1981; Traditionally, the Potamididae included two subfami- Houbrick, 1984; Plaziat, 1984). Three species are recog- lies, Potamidinae and Batillariinae (e.g. Thiele, 1929; nized in the western Atlantic (Bequaert, 1942) and five in Wenz, 1938). However, data on ultrastructure the eastern Pacific (Keen, 1971; Abbott, 1974), although (Healy, 1983), anatomy (Houbrick, 1988; Glaubrecht, distinctions among the latter are not well defined. In the 1996) and DNA sequences (Lydeard et al., 2002) have tropical IWP four species of the subgenus Cerithideopsilla shown that these should be ranked as distinct families that occur (Van Regteren Altena, 1940; Brandt, 1974); C. cingu- are not sister taxa within the . Shell forms can lata lives in dense aggregations on open mudflats of shel- be similar, so that some differences persist in the classifica- tered bays and lagoons that are often, but not tion of fossil members of these families; for example, we necessarily, fringed by mangroves (Vohra, 1970; Balapara- assign Granulolabium to the (Lozouet, 1986; meswara Rao and Sukumar, 1982; Maki et al., 2002), while Lozouet et al., 2001; Harzhauser, 2004) while others still the others are usually found on the mud in the shade of retain it in Potamididae (Kadolsky, 1995; Kowalke, 1998, mangrove trees (Van Benthem Jutting, 1956; Wells, 1985; 2003). As presently understood, the Potamididae consist Maki et al., 2002; DGR, unpublished). In addition, the of five living genera: Potamides, Cerithidea, Terebralia, uncommon and enigmatic species C. largillierti has been Telescopium and Tympanotonos. These each occupy a dis- placed in Cerithidea, although Houbrick (1984) suggested tinct range of microhabitats within mangrove forests, that a new genus was more appropriate; it has been among saltworts, in saltmarsh and on adjacent tidal flats recorded from eastern and (Wilson, 1993; 682 D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699

Hasegawa, 2000) and is found on mud beneath mangroves (Houbrick, 1984, 1991) and even those that inhabit open and saltworts. There is no confirmed fossil record of Ceri- mudflats presumably benefit from the high primary pro- thidea species earlier than the Miocene of the IWP (Hou- ductivity of adjacent mangrove forests and saltmarshes. brick, 1984), although the name has been used for species As reviewed above, the morphology and ecology of in the Eocene of Europe (Cossmann and Pissarro, 1910– many living potamidids are well known and their alpha 1913; Glibert, 1962). is mainly uncontroversial (with the exception The remaining potamidid genera, Tympanotonos, Tele- of some species groups of Cerithidea). The family has a rich scopium and Terebralia, are large, ground-dwelling mud- fossil record but, owing to marked intraspecific variation, whelks, often exceeding 80 mm in length, which resist the morphological convergence and lack of consistent diagno- intense crushing in mangrove habitats by means ses of genera (and even of the family itself), the fossil record of their heavy, armoured shells (Sa¨lgeback and Savazzi, is difficult to interpret. Several subfamilial classification 2006). Numerous fossil species in the Tethys and North schemes have been proposed for living and fossil species America, extending back to the Eocene, have been classi- (Bouniol, 1981; Lozouet, 1986; Bandel, 2006), implying fied as Tympanotonos (e.g. Squires, 1999; Lozouet et al., phylogenetic relationships among genera, but the formal 2001; Kowalke, 2001b, 2003; Harzhauser, 2004). However, phylogeny of the family remains largely unknown. Based the type of the genus and only living species is the West on a parsimony analysis of morphological characters, Hou- African Tympanotonus fuscatus, found on estuarine mud- brick (1984) suggested that Cerithidea was a monophyletic flats and beneath mangroves, with an ecophenotypically group, and in a wider cladistic analysis of the superfamily variable shell (Plaziat, 1977, 1984; Brown, 1994; Bandel Cerithioidea raised this genus to family level (Cerithidei- and Kowalke, 1999). The classification of fossil Tympanot- dae; Houbrick, 1988), as the sister of Potamididae. This onos is in doubt; Lozouet (1986) pointed out a resemblance suggestion was later revoked (Houbrick, 1991). Four pota- to Potamides, whereas Kadolsky (1995) placed some in the midid species (two Cerithidea s. s.,aTerebralia and Tele- genus Mesohalina. The genus Telescopium also contains a scopium) were included in a molecular phylogenetic single living species, and together with three species of Ter- analysis of the superfamily Cerithioidea using the mito- ebralia is abundant among mangroves and on adjacent chondrial 16S rRNA gene and the monophyly of the family mudflats in the central IWP (Houbrick, 1991). There is was moderately supported (Lydeard et al., 2002). The pop- some separation by microhabitat and diet; a combination ulation structure of six taxonomic species of Cerithidea in of consistency of the mud substrate, tidal level and shade Japan has been studied using haplotypes of the mitochon- from the tree canopy determines the relative distributions drial cytochrome c oxidase subunit I (COI), but the mono- of these species (Wells, 1980; Houbrick, 1991; Crowe and phyly of the genus was not tested (Kojima et al., 2006). McMahon, 1997). Only the smallest of them, Terebralia In the present study we aim firstly to examine the molec- sulcata, occasionally climbs onto mangrove roots (Sa¨lge- ular phylogeny of the Potamididae using a much larger back and Savazzi, 2006), and in some areas may gain pro- sampling of taxa (including representatives of all generic tection from predatory rays by living among and subgeneric groups, and 19 of the 29 nominal species), pneumatophores of Avicennia trees (Wells, 1986). Whereas a combination of three genes (18S rRNA, 28S rRNA, most are algal-detritivores like other potamidids, adult COI) and a range of appropriate cerithioidean outgroups. are unique in consuming freshly fallen This has enabled us to test the monophyly of the family Rhizophora leaves (Fratini et al., 2001), although this diet and of the ecologically and taxonomically diverse genus is not obligatory (Feulner, 2000). The fossil record of Tele- Cerithidea, and the hypothesis (implied by the subfamily scopium has not been confirmed before the Miocene; con- classification of Bandel, 2006) that the enigmatic monospe- vergence with members of Campaniloidea casts doubt on cific Potamides is sister to all other potamidids. older claims (Houbrick, 1991). However, shells of - Our second aim is to integrate the molecular phylogeny lia are distinctive, and have been reliably identified in the of living Potamididae with their extensive fossil record and Eocene of Europe (Kowalke, 2001b) and throughout the geographical distributions, to develop an historical biogeo- tropics in the Miocene (Houbrick, 1991). graphic hypothesis. In the absence of any comprehensive In general, therefore, those living potamidids that are survey of potamidid , it has first been necessary to restricted to mangrove habitats appear to depend upon establish a taxonomic framework and to review the exten- the trees for substrate, shelter or food. Some species climb sive primary literature. on the trees or live among roots in order to escape preda- The nature of the remarkable ecological dependence of tion (Cerithidea sensu stricto, some Cerithideopsis, T. sul- living mudwhelks on mangrove environments has been well cata). Spawning has been observed in a minority of documented. Using a molecular phylogeny, and habitat species, but egg strings are commonly attached to hard sub- information for living and fossil species, our third aim is strates including mangrove bark (Houbrick, 1984, 1991; to test the hypothesis that the diversification of extant pot- Bandel and Kowalke, 1999). Some large mudwhelks amidids was contemporary with that of mangroves in the actively seek the shade and humidity beneath the trees Early Eocene, and that specialization to the mangrove (Terebralia). Only T. palustris feeds on mangrove litter, environment is a plesiomorphic feature. This would but the remainder are all algal feeders and detritivores strengthen the case for using fossil potamidids as indicators D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699 683 of palaeomangrove environments (Plaziat, 1995), and for for 3 min at 95 °C, followed by 40 cycles of 45 s at 94 °C, using the family as a model for diversification of the man- 45 s at a gene-specific annealing temperature (Table 2), groves themselves (Ellison et al., 1999; Ellison, 2002). This 2 min at 72 °C, with a final extension of 10 min at 72 °C. hypothesis would be falsified if the basal potamidids were All temperature changes were ramped 1 °C/s. Sequence sediment-dwellers without an obligate mangrove associa- reactions were performed directly on purified PCR prod- tion (such as Potamides and Cerithidea (Cerithideopsilla) ucts using a BigDye Terminator v1.1 Cycle Sequencing cingulata), as implied by one classification scheme (Bandel, Kit (Applied Biosystems) and run on an Applied Biosys- 2006). tems 3730 DNA Analyser automated capillary sequencer. Sequences were verified by forward and reverse compar- 2. Materials and methods isons. Some 18S rRNA and 28S rRNA sequences showed intra-individual variation (heterozygous bases) as has also 2.1. Sampling of taxa been found in other molluscs (Stothard et al., 2000; Bon- naud et al., 2002; Williams and Reid, 2004; Williams The ingroup consisted of 19 species of Potamididae, et al., 2003, 2004; Armbruster and Korte, 2006). In such including representatives of each of the recognized genera cases, two peaks were clearly observed in both forward and subgenera (65% of the 29 taxonomic morphospecies, and reverse chromatograms and were scored as intra-indi- as reviewed above) (Table 1). Where possible, two speci- vidual polymorphism. All sequences have been deposited in mens of each species were sampled from widely separated GenBank (accession numbers 28S rRNA: AM932690– localities, and up to six individuals for particularly wide- AM932749; COI: AM932750–AM932809; 18S rRNA: spread or variable taxa. Nine outgroup taxa were used, rep- AM932810–AM932872). resenting the cerithioidean families , Batillariidae (genera , Lampanella, , ), 2.3. Sequence analysis and phylogeny reconstruction and (Table 1). One of these, Modu- lidae, has been identified as the sister taxon of Potamididae Sequences were edited using Sequencher (v4.5, Gene by a morphological cladistic analysis (Glaubrecht, 1996), a Codes Corporation, Ann Arbor, Michigan). Sequences of relationship neither contradicted nor supported by the only ribosomal genes were aligned using Clustal X (Thompson available molecular phylogeny of the Cerithioidea (Lyde- et al., 1994, 1997) (‘delay divergent sequence’ = 95%, ard et al., 2002). Identifications were based on the most gap-opening penalty = 20, gap-extension penalty = 5) with recent taxonomic accounts (reviewed above). minor adjustments made by eye in MacClade (v4.06 OSX; Maddison and Maddison, 2003). Poorly aligned sites were 2.2. DNA extraction, amplification and sequencing identified using Gblocks (0.19b, Castresana, 2000) and removed from analyses with parameters set as in Williams DNA was extracted from mantle or foot tissue of etha- and Ozawa (2006). After removal of these ambiguous nol-preserved material using a DNeasy Blood and Tissue blocks of data, a total of 971 bp of sequence from 18S Kit (Qiagen) following the manufacturers’ instructions. rRNA remained to be used in phylogenetic analyses (94% Genomic DNA was eluted from the columns in 400 llof of 1030 bp in the original alignment) and 1448 bp of 28S elution buffer. Potamidid DNA required further purifica- rRNA (97% of 1485 bp in the original alignment). tion prior to PCR amplification to remove inhibitors. This Two different methods were used to assess incongruence was achieved by adding 62.5 ll of 5 M NaCl to the DNA, among gene partitions. Firstly posterior probabilities (PP) followed by 50 ll of hexadecyltrimethyl ammonium bro- were compared between trees, with strongly supported mide (CTAB) (10% v/v) in 0.7 M NaCl solution. This was (PP P 95%) clades that conflicted seen as evidence of incubated for 10 min at 68 °C and then extracted with equal incongruence (Wiens, 1998; Reeder, 2003; Williams and volumes of chloroform: iso-amyl alcohol (24:1) and phenol: Reid, 2004). This relies on the argument that weakly sup- chloroform (1:1). The DNA was precipitated with an equal ported clades (PP < 95%) in conflict may be the result of volume of isopropanol, washed with 70% ethanol and dried stochastic error, rather than different phylogenetic histories and resuspended in 100 ll of 10 mM Tris–HCl pH 8. (Wiens, 1998). Secondly, the partition homogeneity test in Portions of three genes were amplified and sequenced: Paup was used to test for incongruence between genes. One the nuclear 18S rRNA and 28S rRNA genes, and the mito- hundred replicates of the ILD were conducted using a heu- chondrial COI gene. Polymerase chain reactions (PCR) ristic search with tree bisection-reconnection branch swap- were used to amplify approximately 1000 bp of 18S rRNA, ping (TBR), random addition of taxa with 10 replicates 1500 bp of 28S rRNA and 700 bp of COI. Reactions con- and the maximum number of trees constrained to 10,000. tained 0.1 lM of a forward and reverse PCR primer (Table All characters were weighted equally, gaps were treated 2), 200 lM of each dNTP, a gene-dependent concentration as fifth characters, and multiple states (in 18S and 28S) of magnesium chloride (Table 2), 2.5 U of Qiagen DNA were treated as polymorphism. The ILD test showed no polymerase (50 ll reaction), one-fifth volume of ‘Q solu- significant incongruence among gene partitions tion’ and one-tenth volume of Qiagen buffer (10). Ther- (P = 0.01), but there were examples of conflict among mal cycling was performed with an initial denaturation well-supported (PP P 95%) basal nodes among trees based 684

Table 1 680–699 (2008) 47 Evolution and Phylogenetics Molecular / al. et Reid D.G. Species of Potamididae (ingroup) and nine outgroup taxa (Thiaridae, Batillariidae, Cerithiidae, Modulidae) used in this study, with geographical ranges, localities of samples, and deposition of voucher material Species Range Sample location and code Voucher material Outgroups cf. amarula (Linnaeus, 1758) IWP. Freshwater 1: Obi, Maluku Utara, ZMB 191.489 Lampanella minima (Gmelin, 1791) W Atlantic 1: Punta Rassa, Florida, USA BMNH 20070368 (Bruguie`re, 1792) NW Pacific 1: St Johns I., BMNH 20070371 (Bruguie`re, 1792) E Australia 1: Sandy Point, S of Mooan, Fraser I., , Australia AMS C411801 (Kiener, 1841) 1: Kulim Park, Otumoetai, Tauranga Harbour, New Zealand MNZ M.181413 Kiener, 1841 Central IWP 1: Lampia, S of Malili, S Sulawesi, Indonesia ZMB 191.634 Bruguie`re, 1792 IWP 1: Panglao, MNHN M3/BC128 Lamarck, 1822 IWP 1: Panglao, Philippines MNHN R14/BC266 modulus (Linnaeus, 1758) W Atlantic 1: Bocas del Toro, Panama BMNH 20050723 Potamididae Potamides conicus (Blainville, 1829) Mediterranean, 1: Khor Zawra, Ajman, United Arab Emirates BMNH 20070406 Indian O. 2: Ibo I., Cabo Delgado Prov., BMNH 20070407 Cerithidea (Cerithidea) anticipata Iredale, 1929 N and NE Australia 1: Thirsty Sound, Porters Creek, just S of Plum Tree, Queensland, Australia. AMS C418805 2: Ludmilla Creek, Darwin Harbour, , Australia ZMB 103.156 3: Sandy Creek, Casuarina Beach, Darwin Harbour, Northern Territory, Australia BMNH 20070372 Cerithidea (Cerithidea) decollata (Linnaeus, 1758) W Indian O. 1: Ibo I., Cabo Delgado Prov., Mozambique BMNH 20070374 2: SE Pemba Bay, Cabo Delgado Prov., Mozambique BMNH 20070375 Cerithidea (Cerithidea) obtusa (Lamarck, 1822)* Indo-Malaya 1: Mekong Delta, BMNH 20070377 Cerithidea (Cerithidea) ornata A. Adams, 1863 W Pacific O. 1: Mouth of Hikawa River, Hikawa Town, Yatsushiro-gun, Kumamoto Prefecture, BMNH 20070378 Kyushu, Japan 2: Sai Kung, Hong Kong BMNH 20070380 3: Sandbyakken, Otsuka, Nakatsu City, Oita Pref., Kyushu, Japan BMNH 20070379 4: Panglao, Philippines MNHN M29/BC1656 Cerithidea (Cerithidea) quadrata Sowerby, 1866 Indo-Malaya 1: Panglao, Philippines MNHN M31/BC1745 2: Panglao, Philippines MNHN M49/BC2153 3: Middle Kung Kraben Bay, Chantaburi Prov., SE BMNH 20070385 4: Ninh Phu, 25 km N of Nha Trang, Vietnam BMNH 20070386 Cerithidea (Cerithidea) rhizophorarum A. Adams, 1855 NW Pacific 1: Mouth of Tamshui River, Bali, N Taiwan BMNH 20070387 2: Makiya, Okinawa, Japan BMNH 20070388 3: Sai Kung, Hong Kong BMNH 20070389 Cerithidea (Cerithideopsis) montagnei (d’Orbigny, 1839) Tropical E Pacific 1: Playa Pochote, Nicoya Peninsula, Costa Rica BMNH 20070413 Cerithidea (Cerithideopsis) valida (C.B. Adams, 1852) Tropical E Pacific 1: Shore opposite Isla Damas, Quepos, Costa Rica BMNH 20070414 Cerithidea (Cerithideopsilla) alata (Philippi, 1849) Indo-Malaya 1: Middle Kung Kraben Bay, Chantaburi Prov., SE Thailand BMNH 20070391 Cerithidea (Cerithideopsilla) cingulata IWP 1: Mouth of Tamshui River, Bali, N Taiwan BMNH 20070398 (Gmelin, 1791)* 2: Sandbyakken, Otsuka, Nakatsu City, Oita Pref., Kyushu, Japan BMNH 20070401 3: Khor Zawra, Ajman, United Arab Emirates BMNH 20070395 4: St Johns I., Singapore BMNH 20070397 5: Thirsty Sound, Plum Tree, Queensland, Australia AMS C419621 6: Lake Alexander, East Point, Darwin Harbour, Northern Territory, Australia BMNH 20070402 Cerithidea (Cerithideopsilla) djadjariensis W Pacific 1: Middle Kung Kraben Bay, Chantaburi Prov., SE Thailand BMNH 20070404 (K. Martin, 1899) 2: Kiire, Kagoshima Pref., Japan ZMB 112.772 3: Sai Kung, Hong Kong BMNH 20070405 4: Ninh Phu, 25 km N of Nha Trang, Vietnam BMNH 20070393 Cerithidea (Cerithideopsilla) microptera Indo-Malaya 1: Panglao, Philippines MNHN M27/BC/675 (Kiener, 1842) Cerithidea largillierti (Philippi, 1848) Japan to Australia 1: River mouth of Jiksocheon, Bulmu-dong, Daehang-ri, Byeonsan-myeon, Buan-gun, BMNH 20070408 Jeonrabuk-do, South Korea 680–699 (2008) 47 Evolution and Phylogenetics Molecular / al. et Reid D.G. 2: Lower reaches of Ushitsu River, Nagata, Ashikari Town, Ogi City, Saga Prefecture, BMNH 20070410 Kyushu, Japan. 3: Plum Tree, Thirsty Sound, Queensland, Australia AMS C419622 4: East Arm, Darwin Harbour, Northern Territory, Australia BMNH 20070412 (Linnaeus, 1758)* W Africa 1: Ankobra River, 70 km W of Takoradi, Ghana BMNH 20070430 2: Old Ningo, 30 km E of Accra, Ghana BMNH 20070431 3: Garta, Gambia R., Gambia ZMB 106.173 (Linnaeus, 1758)* Central IWP 1: Panjim, , ZMB 200.319 2: Middle Kung Kraben Bay, Chantaburi Prov., SE Thailand BMNH 20070415 3: Panglao, Philippines MNHN M30/BC1774 4: Great Sandy Strait, Urangan Sandflats at mouth of Pulgul Creek, Queensland, Australia AMS C411505 5: Ludmilla Creek, Darwin Harbour, Northern Territory, Australia BMNH 20070416 Terebralia palustris (Linnaeus, 1767)* IWP 1: Middle Kung Kraben Bay, Chantaburi Prov., SE Thailand BMNH 20070417 2: Kunduchi Creek, 40 km N Dar es Salaam, BMNH 20070419 3: Ludmilla Creek, Darwin Harbour, Northern Territory, Australia BMNH 20070421 Terebralia semistriata (Mo¨rch, 1852) N Australia 1: Great Sandy Strait, Urangan Sandflats at mouth of Pulgul Creek, Queensland, Australia AMS C448572 2: Ludmilla Creek, Darwin Harbour, Northern Territory, Australia ZMB 103.158 3: Cockle Bay, Magnetic I., Queensland, Australia AMS C448382 (Born, 1778) Central IWP 1: Channel I., Middle Arm, Darwin Harbour, Northern Territory, Australia BMNH 20070425 2: St Johns I., Singapore BMNH 20070424 3: Panglao, Philippines MNHN M6/BC151 4: Panglao, Philippines MNHN M44/BC2117 Taxonomy and ranges from Keen (1971), Abbott (1974), Brandt (1974), Brown (1994), Houbrick (1984, 1991), Kowalke (1998), Lozouet (1986), Wilson (1993), Hasegawa (2000) and Ma (2004). Abbreviations: AMS, Australian Museum, Sydney; BMNH, Natural History Museum, London; IWP, Indo-West Pacific; MNHN, Muse´um National d’Histoire Naturelle, Paris; MNZ, Museum of New Zealand Te Papa Tongarewa; ZMB, Museum fu¨r Naturkunde, Berlin. Type species of potamidid genera and subgenera are indicated by asterisks. 685 686 D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699

Table 2 Forward (F) and reverse (R) PCR primers (also used in sequencing), and forward (FS) and reverse (RS) internal sequencing primers 0 0 Name Sequence 5 -3 Annealing temp. (°C) MgCl2 conc. (mM) Source 18S rRNA 54 3.0 18S-50 (F) CTG GTT GAT YCT GCC AGT Winnepenninckx et al. (1998) 18S1100R (R) CTT CGA ACC TCT GAC TTT CG Williams and Reid (2004) 18S600F (FS) GGT GCC AGC AGC CGC GGT Reverse of 18S600R 18S600R (RS) ACC GCG GCT GCT GGC ACC Modified from Littlewood et al. (2000) 28S rRNA 52 2.5 LSU5 (F) TAG GTC GAC CCG CTG AAY TTA AGC A Littlewood et al. (2000) LSU1600R (R) AGC GCC ATC CAT TTT CAG G Williams et al. (2003) 900F (FS) CCG TCT TGA AAC ACG GAC CAA G Reverse of ECD2S ECD2S (RS) CTT GGT CCG TGT TTC AAG ACG G Modified from Littlewood et al. (2000) LSU330F (FS) CAA GTA CCG TGA GGG AAA GTT G Williams and Ozawa (2006) COI 50 3.0 LCO1490 (F) GGT CAA CAA ATC ATA AAG ATA TTG G Folmer et al. (1994) HCO2198 (R) TTA ACT TCA GGG TGA CCA AAA AAT CA Modified from Folmer et al. (1994)

Annealing temperatures and concentration of magnesium chloride (MgCl2) used in 50 ll polymerase chain reactions.

on single gene datasets (Fig. 1; see Results). Nevertheless, Ronquist, 2001). Models to be used in Bayesian analyses all three genes were concatenated and analysed in a com- were determined by MrModelTest (v2.1, J. Nylander, bined dataset. www.ebc.uu.se/systzoo/staff/nylander.html). In addition, Phylogenies were constructed for each gene-sequence the COI dataset was tested to see whether variation across dataset and for the combined dataset, using Bayesian meth- codon positions would result in an improved likelihood. ods implemented by MrBayes (v3.1.2, Huelsenbeck and The best model for 18S rRNA was SYM + I + G and for

18S rRNA 28S rRNA COI

Thiara cf. amarula 1 Thiara cf. amarula 1 Modulus modulus 1 Modulus modulus 1 Modulus modulus 1 84 Batillaria zonalis 1 52 Pyrazus ebeninus 1 100 Lampanella minima 1 Zeacumantus lutulentus 1 Zeacumantus lutulentus 1 100 80 Zeacumantus lutulentus 1 50 Pyrazus ebeninus 1 100 Batillaria zonalis 1 84 Pyrazus ebeninus 1 Tympanotonos fuscatus 1 100 61 Lampanella minima 1 73 Batillaria zonalis 1 Tympanotonos fuscatus 2 100 Cerithium coralium 1 100 Cerithium nodulosum 1 Tympanotonos fuscatus 3 Cerithium echinatum 1 Cerithium echinatum 1 Cerithium nodulosum 1 Cerithium nodulosum 1 73 Cerithium coralium 1 66 Lampanella minima 1 Cerithidea ornata 1 100 Terebralia palustris 3 Cerithium coralium 1 Cerithidea ornata 2 Terebralia palustris 69 Cerithium echinatum 1 Cerithidea ornata 3 1 Cerithidea ornata 4 100 98 Terebralia palustris 2 99 Cerithideopsilla alata 1 Cerithidea quadrata 1 65 Terebralia semistriata 3 64 Cerithideopsilla microptera 1 Cerithidea quadrata 2 98 Terebralia semistriata 2 100 Cerithideopsilla djadjariensis 3 Terebralia sulcata 1 Cerithideopsilla djadjariensis 4 Cerithidea quadrata 3 74 75 Cerithidea quadrata 4 Terebralia sulcata 2 78 Cerithideopsilla djadjariensis 1 Cerithidea obtusa 1 60 Terebralia sulcata 3 100 Potamides conicus 2 70 Terebralia sulcata 4 Potamides conicus 1 1 85 Cerithidea rhizophorarum 2 100 Telescopium telescopium 1 81 Cerithideopsilla cingulata 6 Cerithidea rhizophorarum 3 100 Telescopium telescopium 4 Cerithideopsilla cingulata 5 Cerithidea anticipata 1 92 Telescopium telescopium 5 85 Cerithideopsilla cingulata 3 Cerithidea anticipata 2 100 89 Telescopium telescopium 2 55 Cerithideopsilla cingulata 2 Cerithidea anticipata 3 100 Telescopium telescopium 3 100 Cerithideopsilla cingulata 1 1 100 Tympanotonos fuscatus 1 99 Telescopium telescopium 5 Cerithidea decollata 2 Tympanotonos fuscatus 2 100 Telescopium telescopium 4 Cerithideopsis largillierti 1 80 100 Cerithideopsis montagnei 1 Telescopium telescopium 1 100 Cerithideopsis largillierti 2 58 100 Cerithideopsis valida 1 78 98 Telescopium telescopium 2 100 Cerithideopsis valida 1 100 Cerithideopsis largillierti 3 98 Telescopium telescopium 3 90 Cerithideopsis montagnei 1 Cerithideopsis largillierti 4 Cerithidea ornata 4 100 Cerithideopsis largillierti 3 Cerithideopsis largillierti 1 Cerithidea obtusa 1 Cerithideopsis largillierti 4 53 70 Tympanotonos fuscatus 1 79 Cerithideopsis largillierti 2 100 Cerithidea anticipata 1 Tympanotonos fuscatus 2 100 Cerithideopsilla alata 1 Cerithidea anticipata 3 73 Telescopium telescopium 2 53 Cerithideopsilla microptera 1 98 99 Cerithidea anticipata 2 Telescopium telescopium 1 100 100 Cerithideopsilla djadjariensis 4 92 100 Cerithidea quadrata 3 100 Telescopium telescopium 3 Cerithideopsilla djadjariensis 1 Cerithidea quadrata 4 Telescopium telescopium 4 98 Cerithideopsilla djadjariensis 3 95 Cerithidea quadrata 1 89 Cerithideopsilla cingulata 4 100 Cerithidea quadrata 2 99 Telescopium telescopium 5 96 52 Terebralia palustris 1 Cerithideopsilla cingulata 3 100 Cerithidea ornata 1 Terebralia palustris 2 8778 Cerithideopsilla cingulata 6 Cerithidea ornata 3 Terebralia palustris 3 Cerithideopsilla cingulata 5 100 Cerithidea decollata 2 100 Cerithideopsilla cingulata 1 72 Cerithidea decollata 1 Terebralia semistriata 1 100 100 Terebralia semistriata 2 Cerithideopsilla cingulata 2 65 Cerithidea rhizophorarum 2 Terebralia semistriata 3 Potamides conicus 2 Cerithidea rhizophorarum 3 67 100 Terebralia sulcata 1 100 Potamides conicus 1 Cerithidea rhizophorarum 1 Terebralia sulcata 2 Cerithidea ornata 4 100 Cerithideopsis montagnei 1 82 Terebralia sulcata 3 99 Cerithidea decollata 2 Cerithideopsis valida 1 Terebralia sulcata 4 100 Cerithidea decollata 1 80 100 Cerithideopsis largillierti 4 100 Potamides conicus 1 Cerithidea obtusa 1 100 Cerithideopsis largillierti 3 Potamides conicus 2 85 50 Cerithidea anticipata 1 100 Cerithideopsis largillierti 1 Cerithideopsilla cingulata 1 Cerithidea anticipata 3 Cerithideopsis largillierti 2 100 Cerithideopsilla cingulata 2 79 Cerithideopsilla cingulata 3 96 Cerithidea quadrata 3 100 Terebralia palustris 3 100 Cerithideopsilla cingulata 4 Cerithidea quadrata 4 Terebralia palustris 1 88 Cerithidea quadrata 1 92 Terebralia palustris 2 Cerithideopsilla cingulata 5 100 96 Cerithideopsilla cingulata 6 100 Cerithidea quadrata 2 99 Terebralia semistriata 3 Cerithidea ornata 1 Terebralia semistriata 2 99 Cerithideopsilla alata 1 96 Cerithideopsilla microptera 1 Cerithidea ornata 3 91 Terebralia semistriata 1 99 Cerithideopsilla djadjariensis 1 100 Cerithidea ornata 2 99 Terebralia sulcata 4 100 Cerithideopsilla djadjariensis 2 Cerithidea rhizophorarum 2 100 Terebralia sulcata 1 Cerithidea rhizophorarum 3 Terebralia sulcata 3 Cerithideopsilla djadjariensis 3 76 76 Cerithideopsilla djadjariensis 4 Cerithidea rhizophorarum 1 93 Terebralia sulcata 2 0.1 substitutions/site 0.05 substitutions/site 0.1 substitutions/site

Fig. 1. Molecular phylogenies of Potamididae produced by Bayesian analysis of datasets from individual genes, the nuclear 18S rRNA (A), 28S rRNA (B) and mitochondrial COI (C). The taxonomy follows the traditional arrangement (Table 1), except that the three subgenera of Cerithidea (Cerithidea s. s., Cerithideopsis, Cerithideopsilla; Houbrick, 1984) are raised to genus rank, and Cerithidea largillierti is assigned to Cerithideopsis. The outgroups are members of Thiaridae, Modulidae, Batillariidae and Cerithiidae (Table 1). Support values are Bayesian posterior probabilities. D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699 687 all other datasets the best model was GTR + I + G, using PP = 96%). Elsewhere, the same generic and subgeneric either the hierarchical log-likelihood ratio test or Akaike’s clades were retrieved as in the nuclear gene trees, but some- Information Criterion (AIC). times with low support. At the specific level, almost all tax- These models were used in all Bayesian analyses, with all onomic species were monophyletic with high support parameters free to vary. In the combined Bayesian analy- (PP = 99–100%). Five individuals of Cerithidea (Cerith- ses, variation was partitioned among genes and gene-spe- ideopsilla) cingulata formed a clade with only 85% support. cific model parameters were used (with all parameters Cerithidea (Cerithidea) ornata was not monophyletic free to vary independently within each partition). In addi- (PP = 92%). tion, each gene was allowed to evolve at a different rate. In the analysis of the dataset of the three genes com- The analysis for each data set was run for 3,500,000 gener- bined, all generic and subgeneric clades recognized in sin- ations, with a sample frequency of 100. The first 15,001 gle-gene analyses were retrieved with maximum support, trees were discarded, so that 20,000 trees were accepted together with the sister relationship between Cerithidea s. after likelihood values had reached a plateau. The datasets s. and subgenus Cerithideopsilla + Potamides conicus,and were analysed in two independent runs, and the final tree between the subgenus Cerithideopsis and Cerithidea largilli- was computed from the combination of accepted trees erti (Fig. 2). Other basal relationships among genera were from each run (a total of 40,000 trees). Convergence not well resolved. In contrast to single-gene analyses Tere- between the two runs was tested by examining the potential bralia was excluded from a large clade containing all the scale reduction factors (PSRF) produced by the ‘sump’ remaining potamidids, but support was marginal command in MrBayes. Support for nodes was determined (PP = 93%). Maximum support was achieved for P. coni- using posterior probabilities (calculated by MrBayes). cus falling within the Cerithideopsilla clade, and in a subc- lade with C. cingulata. Monophyly of each of the two 3. Results nominal species C. cingulata and Cerithidea ornata was not supported. The long branch of Tympanotonos in the Phylogenetic trees constructed from the separate gene COI tree did not adversely affect its placement in the datasets are shown in Fig. 1. Monophyly of the family Pot- three-gene tree; in a Bayesian analysis of the two nuclear amididae was highly supported (posterior probability genes alone (not shown) Tympanotonos appeared in the PP = 100%) in the trees from both nuclear genes, but not same position, as sister to Cerithideopsis plus Cerithidea in the COI tree. The 18S rRNA data (Fig. 1A) resolved largillierti, again without significant support (PP = 53%). all the genera and most of the subgenera of Cerithidea, Relationships between clades within the outgroup can- although often with low support (i.e. PP < 95%). Cerithidea not be tested, but the topology was consistent with mono- s. s. was excluded from a major clade of all the remaining phyly of the families Cerithiidae and Batillariidae (Fig. 2). potamidid species (PP = 99%). Sequences of 18S rRNA were highly conserved within each clade and many species 4. Discussion shared identical sequences (only one of each shared sequence was included in the phylogenetic analyses of this 4.1. Phylogeny and classification of the Recent Potamididae gene and the additional species were added to the tree in Fig. 1A after the analysis). The Potamididae formed a monophyletic group in all The 28S rRNA tree showed higher resolution (Fig. 1B). but one of the analyses (clustering of the potamidid Tym- All recognized generic and subgeneric groups were resolved panotonos with outgroup taxa in the COI tree appears to with 100% support, with one exception. Potamides conicus be an artefact of long-branch attraction). This is consistent clustered within Cerithidea (Cerithideopsilla) (PP = 100%; with both anatomical (Healy, 1983; Houbrick, 1988; Pon- in the 18S rRNA tree these two taxa formed a clade but der, 1991; Glaubrecht, 1996) and molecular (Lydeard their relationships were unresolved). The subgenus Cerit- et al., 2002) evidence separating the family from the super- hideopsis was sister to Cerithidea largillierti (subgenus pre- ficially similar Batillariidae, here falling well within the out- viously unspecified; Houbrick, 1984), and Cerithidea s. s. group. Shell characters distinguishing these families have and Cerithideopsilla + Potamides formed a clade with not yet been rigorously defined; they include the twisted 100% support. Other relationships among clades were not columellar base and more rounded of Potamidi- resolved. dae and the secondary spiral of Batillariidae The COI data provided finer resolution at shallow nodes (used by Lozouet, 1986, to distinguish Potamides from (Fig. 1C). Tympanotonos appeared on a long branch in the the batillariid Granulolabium), whereas protoconch charac- COI tree (but not in either of the nuclear gene trees), and ters are not known to be diagnostic (cf. Lozouet, 1986; long-branch attraction (Bergsten, 2005) probably accounts Kowalke, 1998; Bandel, 2006). for the placement of Tympanotonos among the outgroup Within the Potamididae, our molecular phylogenetic taxa. Potamides conicus again fell within Cerithidea hypothesis shows each of the traditional genera Terebralia, (Cerithideopsilla), but without significant support Telescopium and Tympanotonos (Houbrick, 1991)tobe (PP = 78%). This clade was excluded from a large clade monophyletic, and also supports two of the three subgener- of all the remaining potamidids (except Tympanotonos; aofCerithidea (Cerithidea s. s. and Cerithideopsis; Hou- 688 D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699

Fig. 2. Molecular phylogeny of Potamididae produced by Bayesian analysis of combined dataset from concatenated sequences of the nuclear 18S rRNA and 28S rRNA genes and mitochondrial COI gene. The taxonomy follows the traditional arrangement (Table 1), except that the three subgenera of Cerithidea (Cerithidea s. s., Cerithideopsis, Cerithideopsilla; Houbrick, 1984) are raised to genus rank, and Cerithidea largillierti is assigned to Cerithideopsis. The outgroups are members of Thiaridae, Modulidae, Batillariidae and Cerithiidae (Table 1). Support values are Bayesian posterior probabilities. Geographical ranges are indicated; those species without a range occur only in the Indo-West Pacific (IWP) region. Shells: A, Terebralia palustris;B,Telescopium telescopium;C,Tympanotonos fuscatus;D,Cerithideopsis montagnei;E,Cerithideopsis largillierti;F,Cerithideopsilla cingulata;G, Potamides conicus (Cerithideopsilla conica herein); H, Cerithidea obtusa. brick, 1984). However, there is no agreement with any pre- gested that Cerithidea was a monophyletic group of three vious schemes of phylogenetic relationship or subfamilial subgenera, of which Cerithideopsis and Cerithidea s. s. were classification of these living genera. Based on a parsimony sister taxa. Houbrick (1988) named this group as a separate analysis of morphological characters, Houbrick (1984) sug- family, Cerithideidae, sister to the remaining Potamididae, D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699 689 but subsequently reversed this decision, recognizing their this species is retrieved with high support as sister to Cerit- anatomical similarity (Houbrick, 1991). In the present hideopsis and there is a close resemblance between their analysis the two subgenera Cerithidea s. s. and Cerithideop- shells (Table 3). We therefore transfer ‘Cerithidea’ largilli- silla (with the inclusion of P. conicus) are sister taxa, and erti to Cerithideopsis. Diagnostic shell characters for Ceri- there is no support for the addition of Cerithideopsis to this thidea, Cerithideopsilla and Cerithideopsis are summarized group, these basal relationships being unresolved. Modify- in Table 3, and these taxon names will be used at generic ing an earlier scheme of Bouniol (1981) based on similarity rank in the following discussion. of shells, Lozouet (1986) removed Terebralia from the At the species level, our analyses support the classifica- remaining Potamididae, allying it with genera now recog- tion of living Terebralia in three species (Houbrick, nized as batillariid (Zeacumantus and the fossil Granulola- 1991). Three specimens of Tympanotonos fuscatus also bium). This distinction of Terebralia has a parallel in its showed little genetic difference. However, genetic structure marginally supported basal position within Potamididae was found in the nominal species Telescopium telescopium, in the analysis of the combined-gene dataset, but Batillar- with separation of specimens from the Philippines, Austra- iidae are unrelated. Bandel (2006) recognized two subfam- lia and India, and genetic distances (Kimura two-parame- ilies, Potamidinae and Telescopiinae, the latter including ter K2P divergence in COI sequence) of up to 16%, so all living potamidids except Potamides.IfP. conicus is further investigation is required. K2P divergence between accepted as a representative of the former subfamily, then Cerithideopsis largillierti from Japan and from Australia our molecular results contradict this scheme; if not, then averaged 15% and together with a disjunct distribution the placement of all living potamidids into a single group (DGR, unpublished) suggest that two species are involved. has no implication for the phylogenetic relationships Within C. cingulata the K2P divergence between samples among them. In the only previous molecular phylogenetic from Australia and Japan was 14%, suggesting that this study of potamidid genera, Lydeard et al. (2002) reported widespread species may be a complex. The sample of Cer- moderate support (bootstrap 87%) for a sister relationship ithidea ornata from the Philippines did not form a clade between Telescopium and Terebralia, to the exclusion of with those from Japan and Hong Kong in either 28S or Cerithidea s. s. This is contradicted with marginal support COI trees, and therefore do not belong to the same phylo- (PP = 93%) in the present three-gene analysis. genetic species. Despite close morphological similarity, The genus Cerithidea sensu lato contains 23 (79%) of the Cerithidea anticipata from Australia is distinct from C. 29 nominal species of the Potamididae. There is no support quadrata from , judged by consistent phylo- for the monophyly of this large group in our analyses; genetic separation and the average K2P distance for COI of instead, there are three well-supported and genetically 14%. divergent clades, two of which are relatively distant sister taxa (Fig. 2). We suggest that these relationships are best 4.2. Phylogeny, historical biogeography and the fossil record expressed by recognizing three genera, corresponding to of Potamididae the subgenera of Houbrick (1984). Cerithidea s. s. includes ten morphospecies (Brandt, 1974; Wilson, 1993; Brown, The Potamididae have a rich fossil record, but its inter- 1994; Hasegawa, 2000; Ma, 2004), all from the Indo-West pretation is hampered by the lack of direct comparison Pacific (IWP), of which we sampled six (including the type between living and fossil representatives and absence of species C. obtusa). Our analyses included all four morpho- clear generic definitions. A comprehensive revision is species assigned to Cerithideopsilla, all from the IWP (Van beyond the scope of this work, but we have attempted to Regteren Altena, 1940; Brandt, 1974), and to these we add unify the classification of the living genera and those fossils ‘Potamides’ conicus, hitherto the only recognized living spe- that can confidently be assigned to the family (Table 3). cies of its genus (Lozouet, 1986; Plaziat, 1993; Kowalke, Our classification is based on the six monophyletic groups 2001a). As discussed below, the generic name Potamides distinguished in the molecular phylogeny and recognized as is based on a fossil that we consider unrelated to Cerith- genera (see above). These have been diagnosed by charac- ideopsilla. (The generic name Gray, 1847 is based ters of the shell (observations of all living species in Natural on P. conicus, and has priority over the name Cerithideop- History Museum, London, by DGR) and mode of develop- silla Thiele, 1929; nomenclatural research might confirm ment, to provide a framework applicable also to fossil that the former is the valid name for this genus, but would material. Detailed characters of the protoconch and early run counter to current usage.) Our sampling of Cerithide- teleoconch sculpture may prove still more informative opsis is incomplete, including only two eastern Pacific spe- (e.g. Lozouet, 1986; Kadolsky, 1995; Kowalke, 1998), but cies of the approximately eight in the eastern Pacific and remain unavailable for the majority of both living and fos- Atlantic (EPA) provinces (Keen, 1971; Abbott, 1974). sil taxa. The poor basal resolution of the phylogeny of Pot- The shells of this group are closely similar, and we predict amididae, and uncertainty about its immediate sister that further sampling will confirm their monophyly. We group, prevent us from distinguishing apomorphic and ple- have also sampled the enigmatic ‘Cerithidea’ largillierti siomorphic characters (but see discussion of developmental from the IWP; this, according to Houbrick (1984), did mode below). We have made an extensive survey of the fos- not fit into any of his proposed subgenera. In our analyses sil literature and have also examined specimens (in Natural 690 D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699

Table 3 Revised classification of the Potamididae, with principal synonyms and subgroups, and diagnostic shell characters Genus Subgenera or synonyms Shell characters Terebralia ?aGravesicerithiumb Charpiat, 1923a Development: planktotrophic (Houbrick, 1991; Kowalke, 1998, 2001b, 2006a,b; Harzhauser Swainson, 1840 and Kowalke, 2001) aCerithideops Pilsbry and Harbison, whorls: 4 or more spiral ribsc; axial folds, becoming weak; scattered varices with 1933 internal teeth; usually a fold (absent in Cerithideops see Pilsbry and Harbison, 1933, weak in T. subcorrugata see Lozouet, 1986) Ventrolateral : present Aperture: flared; shoulder sinus weak or absent; basal projection may enclose anterior canal Telescopium Development: planktotrophic (Houbrick, 1991) Montfort, 1810 Spire whorls: 3 spiral ribs plus intercalated riblet on shoulder; no axial sculpture except for beading on posterior rib of early whorls; no varices; columella fold Ventrolateral varix absent Aperture: unmodified; indeterminate growth; broad shallow shoulder sinus; basal projection; anterior canal short Tympanotonos Development: planktotrophic (Egonmwan and Odiete, 1983; Bandel and Kowalke, 1999 Schumacher, illustrated the protoconch of a species of Cerithiopsidae in error) 1817 Spire whorls: 3 spiral ribs strongly beaded by axial folds; 1 riblet intercalated between two anterior ribs and another between anterior rib and suture; shoulder rib enlarged or spinose; scattered varices with internal teeth; small columella fold Ventrolateral varix: absent Aperture: flared; broad shallow shoulder sinus; basal projection aPotamides aPtychopotamides Saccho, 1895 Development: mostly non-planktotrophic (Lozouet, 1986; Kadolsky, 1995; Harzhauser and Brongniart, 1810 aMesohalina Wittibschlager, 1983 Kowalke, 2002; lecithotrophic reported by Kowalke, 2001a,b, 2006a,b); 2 reports of planktotrophic development (Reichenbacher et al., 2004) aVicarya d’Archiac and Haime, Spire whorls: 3 spiral ribs, sometimes with intercalated riblets; ribs usually granular or 1854 tubercular; posterior rib may be enlarged or spinose; no varices; columella fold present or absent aVicaryella Yabe and Hatai, 1938 Ventrolateral varix: absent ?aEotympanotonus Chavan, 1952 Aperture: usually flared and thickened; strong shoulder sinus, sometimes very deep (Vicarya); posterior canal, sometimes expanded and callused aCampanilopsis Development: unknown. Chavan, 1949 Spire whorls: 4 spiral ribs, finely granular; posterior rib enlarged, spinose in adult; columella fold Aperture: not flared aPotamidopsis Development: planktotrophic and non-planktotrophic (PL, unpublished). Munier- Spire whorls: 3 granulose spiral ribs; anterior rib enlarged, carinate or spinose; no varices; Chalmas, columella fold? 1900 Ventrolateral varix: absent Aperture: flared and thickened; strong shoulder sinus Cerithideopsis ?aHarrisianella Olsson, 1929 Development: lecithotrophic (Houbrick, 1984) or planktotrophic (C. douvillei, PL, Thiele, 1929 unpublished; Harrisianella vulcani, Kowalke, 2001a,b) ?aLagunitis Olsson, 1929 Spire whorls: 2–3 spiral ribs on earliest whorls, usually becoming obsolete, sometimes increasing to 5; numerous axial folds, terminating at strong spiral rib demarcating the base; scattered varices; no columella fold (present in H. peruviana Olsson, 1929) Ventrolateral varix: absent Aperture: slightly or strongly flared and thickened; peristome weakly sinuous or planar; slight anterior canal Cerithideopsilla Pirenella Gray, 1847d Development: planktotrophic (C. cingulata and C. djadjariensis, Houbrick, 1984) or non- Thiele, 1929 planktotrophic (C. conica, Lozouet, 1986; Kowalke, 2001a) Spire whorls: 3 spiral ribs; numerous axial folds; no varices; no columella fold Ventrolateral varix: present (except C. conica) Aperture: slightly or strongly flared and thickened; peristome weakly sinuous or planar; basal projection defining anterior canal; posterior canal, sometimes forming wing-like projection Cerithidea Development: C. rhizophorarum probably non-planktotrophic (Houbrick, 1984) Swainson, 1840 Spire whorls: earliest whorls decollate; 0–18 spiral ribs on adult whorls; numerous axial folds; no varices; no columella fold Ventrolateral varix: present Aperture: flared and thickened; peristome planar; slight anterior canal a Exclusively fossil genera. b According to Lozouet (1986). c Not counting rib to which succeeding is attached. d Synonymy based on molecular results; type species is Cerithium mamillatum Philippi = Pirenella conica; Pirenella has priority over Cerithideopsilla; see text. ? Indicates doubtful generic assignment. D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699 691

History Museum, London, by DGR; in Muse´um National The earliest fossils that have been assigned to the Pota- d’Histoire Naturelle, Paris, by PL). As a result, we propose mididae include the genera Echinobathra, Hadraxon and new synonymies and diagnoses for some fossil genera and Terebraliopsis (Bandel and Riedel, 1994; Kowalke and question the assignment of some fossils to Recent groups Bandel, 1996; Kowalke, 2003) from the Late Cretaceous. (Tables 3 and 4), as briefly discussed below. However, without a clear diagnosis of the family and with

Table 4 Outline of the fossil record of the Potamididae Taxa Age Geographical range References Echinobathra, Hadraxon, Terebraliopsis L Cret: Alps, Pyrenees Bandel and Riedel (1994); Kowalke and Bandel Maastrichtian (1996); Kowalke (2003) Genus Terebralia ?T. pathani Iqbal, 1969 E Eoc Pakistan Iqbal (1969) T. subcorvina (Oppenheim, 1894) M Eoc: Lutetian Hungary, Italy Kowalke (1998, 2001b) T. bonellii (Deshayes, 1833) M Eoc: Lutetian France Cossmann and Pissarro (1902, 1910–1913) T. vielensis Belliard et al., 2006 M Eoc France Belliard et al. (2006) T. bidentata (Defrance in Grateloup, 1832) L Olig–M Mioc France to Pakistan, Vredenburg (1925); Harzhauser and Kowalke Paratethys (2001, 2002); Lozouet et al. (2001); Harzhauser (2004) T. rahti (Braun, 1851) L Olig–E Mioc Mainz Basin, Aquitaine Kadolsky (1995) Basin T. dentilabris (Gabb, 1873) E Mioc Panama, Florida Woodring (1959); Hoerle (1972) T. shibatai Taguchi, 1992 Mioc Japan Taguchi (1992) Cerithidea (Cerithideops) insulaemaris Pilsbry and Mioc Eastern USA Pilsbry and Harbison (1933) Harbison, 1933 T. palustris (Linnaeus, 1767) E Mioc–Rec IWP; Italy (L Mioc) Van Regteren Altena (1942); Houbrick (1991) Genus Telescopium T. schencki Hatai and Nishiyama, 1949 L/M Mioc Japan Oyama (1950); Shimizu and Kaneko (1992) T. telescopium (Linnaeus, 1758) M Mioc–Rec W Pacific Van Regteren Altena (1942); Houbrick (1991); Inoue (2007) Genus Tympanotonos T. fuscatus (Linnaeus, 1758) Rec W Africa Bandel and Kowalke (1999); Kowalke (2001b) Genus Potamides ?Terebralia juliana Dailey and Popenoe, 1966 L Cret California Dailey and Popenoe (1966) P. (Eotympanotonus ?) n. sp. E Palaeo Oise, France Bouniol (1981) ?Tympanotonos varians (Briart and Cornet, 1873) E Palaeo Belgium Glibert (1973) P. (Ptychopotamides) cinctus (Bruguie`re, 1792) M Eoc Paris Basin Cossmann and Pissarro (1910–1913) Tympanotonus conarius (Bayan, 1873) M Eoc Paris Basin Cossmann and Pissarro (1910–1913) Tympanotonos calcaratus (Brongniart, 1823) M Eoc Hungary Kowalke (2001b) Vicaryella spp. Eoc Pakistan, Indonesia, Japan Kanno (1986) Potamides spp. M Eoc–Plioc Europe Lozouet (1986); Nury (1998); Kowalke (2001a); Harzhauser and Kowalke (2002) P. lamarkii (Brongniart, 1810) E Olig Paris Basin Lozouet (1986) P. suprasulcatus (Gabb, 1873) L Olig–M Mioc Peru–Florida Woodring (1959); Hoerle (1972) Tympanotonos margaritaceus (Brocchi, 1814) L Olig–E Mioc Mainz Basin, France, Kadolsky (1995) (as Mesohalina); Lozouet et al. Greece, , (2001); Harzhauser (2004) Vicarya spp. Mioc Pakistan, W Pacific, Japan Kanno (1986) Genus Potamidopsis Potamides (Potamidopsis) tricarinatus (Lamarck, M Eoc Paris Basin Cossmann and Pissarro (1910–1913) 1804) Potamides (Potamidopsis) californica Squires, 1991 M Eoc California Squires (1991) Tympanotonos trochlearis (Lamarck, 1804) E Olig Paris Basin Gitton et al. (1986) Genus Campanilopsis Telescopium lemniscatum (Brongniart, 1823) M Eoc–E Olig Europe Cossmann (1906); Lozouet (1986) Genus Cerithideopsis Cerithidea (Harrisianella) vulcani (Brongniart, 1823) M Eoc Italy, Hungary Kowalke (2001b) ?Tympanotonos californicus Squires, 1999 M Eoc California Squires (1999) Potamides (Cerithidea) subpunctatus (Deshayes, 1833) M Eoc Paris Basin Cossmann and Pissarro (1910–1913) Potamides (Cerithidea) douvillei (Vasseur, 1882) M Eoc Cotentin, Loire Cossmann and Pissarro (1902); Cossmann (1906) ?Harrisianella peruviana Olsson, 1929 L Eoc Peru Olsson (1929) ?Lagunitus peruvianus Woods, 1922 L Eoc Peru Woods (1922); Olsson (1929) (continued on next page) 692 D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699

Table 4 (continued) Taxa Age Geographical range References Cerithidea (Cerithideopsis) pliculosa (Menke, 1828) Plioc Florida Olsson and Harbison (1953) Genus Cerithideopsilla Cerithidea (Cerithideopsilla) cingulata (Gmelin, 1791) M Mioc–Rec Indonesia, W Pacific Van Regteren Altena (1942); Houbrick (1984); Inoue (2007) Potamides graecus (Deshayes, 1832) M Mioc–Plioc Mediterranean Lozouet (1986); Kowalke (2001a) Genus Cerithidea Cerithidea cf. obtusa (Lamarck, 1822) Mioc Saipan, W Pacific Ladd (1972); Houbrick (1984) Cerithidea (Cerithidea) obtusa Plioc Java Van Regteren Altena (1942) Potamides (Cerithidea) babylonicus Martin, 1884 Plioc Java Martin (1884)

The records are not complete, but attempt to list earliest reliable occurrences of all Recent and some fossil genera, and records demonstrating the full geographical range. Names are those used in the references quoted; revised generic assignment (bold) follows definitions in Table 3. ? Indicates uncertain generic placement. Abbreviations: Cret, Cretaceous (65.5–145.5 Ma); E, Early; Eoc, Eocene (34–56 Ma); L, Late; M, Middle; Mioc, Miocene (5–23 Ma); Olig, Oligocene (23–34 Ma); Palaeo, Palaeocene (56–65.5 Ma); Plioc, Pliocene (1.8–5 Ma). no obvious similarity to Recent genera, their relationships comparative study may reveal that some of these groups cannot yet be assessed. should be recognized as genera, but we believe that they Of the Recent genera, Terebralia is large and distinctive, form a group more closely related to each other than to and has the most complete fossil record (Table 4). The ear- any Recent potamidids (Table 3). Those species of Pota- liest unquestioned member is T. subcorvina from the Mid- mides for which protoconchs have been described were dle Eocene of Europe (Kowalke, 2001b). A poorly mainly non-planktotrophic (Table 3). This is an additional preserved, doubtful species has been described from the distinction from the Recent Tympanotonos, which is plank- Lower Eocene of Pakistan (Iqbal, 1969), but older species totrophic (Egonmwan and Odiete, 1983). Potamides from California do not conform to our generic definition became extinct in the western Pacific (as Vicarya, Kanno, (Dailey and Popenoe, 1966; Squires and Kennedy, 1998). 1986) and in North America (Hoerle, 1972) in the Middle The genus did occur reliably in the during the Miocene, but in Europe continued until the Pliocene (e.g. Miocene, persisted in Europe until the Late Miocene, and P. granosus; Lozouet, 1986). No Recent members of this occurred in the IWP from the Miocene onwards (Table 4). group are known (see discussion of ‘P.’ conicus below). The type species of the genus Tympanotonos is the living We retain Potamidopsis as a distinct genus (Lozouet, T. fuscatus, but the generic name has been widely applied 1986; but listed as a of ‘Tympanotonos’by to fossil species. So too has Potamides, with the Oligocene Kowalke, 2003), with a range from the Middle Eocene to fossil P. lamarkii as type species. Lozouet (1986) first the Early Oligocene (Table 4) and a possible relationship pointed out that these could not be separated as distinct to Potamides. We also consider the enigmatic Tethyan groups, and included Eotympanotonus and Ptychopota- Campanilopsis to be a distinct genus (as subgenus of Tele- mides as subgenera. However, significant sculptural differ- scopium in Lozouet, 1986; listed as a synonym of ‘Tympa- ences (the single largest and sometimes spinose ribs are notonos’byKowalke, 2003). not homologous, and varices are present only in T. fusca- Of the remaining potamidid genera, the Recent Telesco- tus) suggest that Recent and fossil ‘Tympanotonos’ are pium, Cerithidea and Cerithideopsilla are all known no ear- not congeneric, leading Wittibschlager (1983; see also lier than the Miocene and only from the IWP. Kadolsky, 1995) to propose Mesohalina for the Oligocene Cerithideopsis has an older fossil record, one of the earliest ‘Tympanotonos’ margaritaceus. Although this has not been being C. douvillei from the Middle Eocene of the Paris followed by most recent authors (Lozouet, 1986; Lozouet Basin, here assigned to this genus for the first time (shell et al., 2001; Harzhauser and Kowalke, 2001; Kowalke, characters as in Table 3; protoconch indicates plankto- 2003; Harzhauser, 2004), we support this distinction, trophic development; PL, unpublished). The contempora- restricting Tympanotonos to the Recent species and using neous Harrisianella vulcani also appears to belong to Potamides for the fossils. A possible early member of Pot- Cerithideopsis,andKowalke (2001b) earlier noted this amides is ‘Terebralia’ juliana from the Late Cretaceous of resemblance. It remains unclear whether the type species California (Dailey and Popenoe, 1966). The subgenus of Harrisianella from the Upper Eocene of Peru (Olsson, Eotympanotonus may have been present in Europe as early 1929) can also be classified in Cerithideopsis, and an Oligo- as the Early Palaeocene (Bouniol, 1981) and by the Eocene cene species of Harrisianella (Glibert, 1973) is considered was widespread in the Tethyan realm (Table 4). Contempo- an unlikely member. After the Eocene, no fossil Cerithide- raneous shells from the western Pacific have been classified opsis are known until the Pliocene, in the western Atlantic as Vicaryella, apparently based on geographical criteria (Olsson and Harbison, 1953; Houbrick, 1984). rather than morphological difference. The Miocene genus To summarize, the oldest undoubted members of Recent Vicarya from the same region is superficially distinctive, potamidid genera are from the Middle Eocene, when both but differs only in the more enlarged spines of the posterior Terebralia and Cerithideopsis occurred in the European rib and a more expanded aperture (Kanno, 1986). Detailed Tethyan realm (sensu Harzhauser et al., 2002), and the lat- D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699 693 ter genus perhaps also in the Americas. Because the basal 2001a; but see Collin et al., 2007) are rare in gastropods, branches of the molecular phylogeny are not resolved, this we exclude a non-planktotrophic member of Potamides fossil evidence is consistent with the origin of all the Recent from the ancestry of the living potamidids. This, and the genera (and of the clade Cerithidea plus Cerithideopsilla)at older fossil record of Potamides than of Recent genera, sug- or before this time. Terebralia persisted in Europe, and gests the hypothesis that the extinct genera may be sister to reached the western Atlantic in the Early Miocene, when (or paraphyletic to) the monophyletic radiation of the a well-documented migration across the Atlantic took extant Potamididae. This recalls the separation of the two place (Harzhauser et al., 2002). During the Late Miocene subfamilies (Potamidinae and Telescopiinae) advocated Terebralia became extinct in both the Americas and Eur- by Bandel (2006). More detailed study of the fossil taxa ope, and survived only in the IWP. A similar pattern of is required to test this suggestion. widespread distribution followed by restriction to the IWP is common in molluscs and other marine groups (Pau- 4.3. Origin and relationships of ‘Potamides’ conicus lay, 1997; Vermeij, 2001; Williams, 2007). For Cerithideop- sis the combination of phylogenetic and fossil evidence In several respects ‘Potamides’ conicus (as Pirenella con- suggests a different history. It may have been widespread ica before Kadolsky, 1984 and Lozouet, 1986) stands out in both the Tethyan realm and the Americas (if identifica- as an unusual member of the Potamididae, and has there- tions in Table 4 are correct) by the Middle Eocene, when fore been a focus of interest. It extends further north than other trans-Atlantic similarities are also recognized (Ver- most other potamidids (to 40°N in the Mediterranean); it is meij, 2001; Harzhauser et al., 2002). Cerithideopsis now not associated with mangrove habitats, but occupies mar- survives in the AEP and IWP. Our finding of a sister rela- ine lagoons and saline lakes; it is remarkably euryhaline tionship between the radiation of Cerithideopsis in the AEP (5–280‰); development is direct (Lozouet, 1986; Plaziat, and C. largillierti in the IWP suggests historical vicariance. 1993). In keeping with its isolated populations in extreme Possible causes include global cooling at the end of the environments, it shows remarkable shell variation, yet the Eocene or early Miocene aridity, which restricted the man- consensus is that there is only a single species distributed groves of the Tethyan realm (Plaziat et al., 2001) or the in the western Indian Ocean and eastern Mediterranean final closure of the Tethyan corridor at the end of the Early (Lozouet, 1986; Plaziat, 1993; Kowalke, 2001a). (Our sam- Miocene (Harzhauser et al., 2002). A more fully resolved ples were from Mozambique and Arabia; protoconchs were phylogeny and better fossil record might distinguish among not present, but we have confirmed that other Arabian these alternatives. Although the living West African Tym- specimens do have protoconchs like those described from panotonos fuscatus has been considered the sole relict of a the Mediterranean by Kowalke, 2001a, indicating direct formerly pantropical genus (e.g. Kowalke, 2001a,b, development.) Several hypotheses have been proposed to 2003), we have found no evidence of this genus in the Euro- explain this unusual distribution. Por (1978) considered pean fossil record. This is surprising, in view of faunistic Pirenella conica to be a recent (but still ‘pre-Lessepsian’) similarities between Europe and West Africa in the Mio- migrant from the Red Sea, which was able by virtue of cene (Bre´bion, 1974; Lozouet and Gourgues, 1995). For its physiological tolerance to disperse northward through the remaining Recent genera (Telescopium, Cerithideopsil- the hypersaline lakes that were present during the Quater- la, Cerithidea) the limited fossil evidence is consistent with nary before the construction of the Suez Canal. In contrast, origin and radiation within the IWP and (as in Terebralia) Lozouet (1986) identified the species as the sole extant appearance of living species in the Miocene, but the mod- member of the genus Potamides, proposing a line of des- ern restriction of these groups to the IWP might also be cent from the Oligocene P. lamarkii to Miocene P. theodis- the product of extinction elsewhere. cus to Pliocene P. graecus to Recent P. conicus, entirely The relationships of the extinct genera Potamides, Pota- within the Tethyan and Mediterranean region. The pres- midopsis and Campanilopsis to each other and to the ence of P. conicus in the Indian Ocean was considered most Recent potamidid genera remain unclear. The limited evi- likely the result of dispersal, perhaps by birds, dence available suggests that most Potamides species were through the hypersaline lakes of Suez, but in a southward characterized by non-planktotrophic development (Table direction. By implication, the ancestors of P. conicus like- 3). Based on the topology of the phylogeny constructed wise had direct development and were similarly euryhaline, from three genes (Fig. 2), the known developmental modes enabling them to survive in the Mediterranean through the of some of the living species (Table 3), and the preponder- Messinian salinity crises during the Late Miocene. ance of planktotrophic development in other marine ceri- Kowalke (2001a) described the protoconchs of the sup- thiodean families (e.g. , Cerithiidae, posed ancestors of P. conicus, and argued that the lecitho- Modulidae; Kowalke, 1998; Bandel, 2006) that are appro- trophic (i.e. brief planktonic but non-feeding) development priate for outgroup comparison, it can be argued that the of P. theodiscus precluded it from direct ancestry of the ancestor of the living potamidids had planktotrophic devel- planktotrophic P. graecus. He did not, however, question opment. Given that poecilogony (alternative modes of lar- the Tethyan–Mediterranean origin of P. conicus, its recent val development; Ellingson and Krug, 2006) and spread to the Indian Ocean (said to be due to human evolutionary reacquisition of feeding larvae (Kowalke, agency) or its membership of Potamides. 694 D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699

The molecular phylogeny, in combination with the fossil Retention of the morphological hypothesis of descent of record, supports an entirely different hypothesis. ‘Pota- ‘Potamides’ conicus from P. lamarkii, in the light of the mides’ conicus is a member of the otherwise exclusively molecular hypothesis, would require parallel gain of the IWP Cerithideopsilla clade and, in the three-gene tree, clus- ventrolateral varix in Cerithidea and in two to four lineages ters with C. cingulata (internal relationships not resolved, of Cerithideopsilla, as well as multiple invasion of the IWP Fig. 2). A parsimony argument (see above and Table 3) (or multiple extinction in the Mediterranean) to produce suggests that the common ancestor of these two species the biogeographic pattern (Fig. 2). We consider this unten- was a planktotrophic inhabitant of the IWP (like C. cingu- able. Nevertheless, our hypothesis remains to be fully lata; Houbrick, 1984). Our new interpretation of the fossil tested by a more detailed study of the fossil record, and record is that P. theodiscus was the last of the direct-devel- by molecular sampling of C. conica from the Mediterra- oping P. lamarkii–P. theodiscus lineage in the Mediterra- nean to confirm that it is conspecific with Indian Ocean nean, becoming extinct in the Paratethys during the Late populations. Miocene. Although it would be most parsimonious to con- clude that ‘P.’ conicus arose in the IWP and dispersed northward to the Mediterranean, the fossil record suggests 4.4. Evolution of Potamididae and the mangrove habitat otherwise. ‘Potamides’ graecus is a candidate for the plank- totrophic ancestor of ‘P.’ conicus; the latter must therefore It is a longstanding question whether mangrove forests have originated in the Mediterranean, and both should be have a characteristic fauna of species that show a strict classified as Cerithideopsilla. In support of this reclassifica- association with this habitat (Plaziat, 1984; Glaubrecht, tion, C. graeca shows a weak ventrolateral varix (PL, 1997; Plaziat et al., 2001). As reviewed above, all the living unpublished), present in IWP Cerithideopsilla but absent genera of Potamididae are associated with mangroves, in all Potamides (Table 3), suggesting how this was reduced using the trees for shelter, as a substrate, for food and pro- and lost in C. conica, resulting in the convergence of the lat- tection from predators. A dietary specialization is shown ter with Potamides species. Cerithideopsilla graeca was by Terebralia palustris, which as an adult feeds on fallen planktotrophic and thus likely to have been a species of Rhizophora leaves using a specially modified (Plazi- marine or brackish habitats like IWP Cerithideopsilla (the at, 1977; Houbrick, 1991; Fratini et al., 2001), yet popula- salinity tolerance of C. cingulata is 1.5–50‰, Vohra, tions in Arabia exist without this food source and even 1970; Plaziat and Younis, 2005). We therefore suggest that survive in sheltered habitats without mangrove trees (Feul- C. graeca reached the Mediterranean either before the clo- ner, 2000). Similarly, although Cerithidea species typically sure of the Tethyan–Indian Ocean connection at the end of climb mangrove trees, they can exist locally on saltwort the Early Miocene (late Burdigalian) or during the inter- vegetation and driftwood (DGR, unpublished). Neverthe- mittent connections of the Middle Miocene (Harzhauser less, it is true that most living potamidid species maintain et al., 2002). The earliest record of C. graeca is from the their greatest numbers on or beneath mangrove trees and Late Miocene of Greece (Tortonian; Kowalke, 2001a), sug- probably could not survive without them. There are at least gesting the latter alternative. (The taxonomy and relation- three exceptions. In the IWP, Cerithideopsilla cingulata is ships of the fossil Cerithideopsilla require reexamination; abundant on sheltered, intertidal, muddy sandflats that some Pliocene examples of C. graeca from Tunisia have are not necessarily adjacent to mangroves (Vohra, 1970; non-planktotrophic development, PL unpublished, empha- Balaparameswara Rao and Sukumar, 1982; Maki et al., sizing the likely descent of C. conica. Furthermore, Lozou- 2002; Plaziat and Younis, 2005). In the Mediterranean et, 1986, mentioned another Cerithideopsilla-like Pliocene and Indian Ocean, C. conica occupies a similar habitat species, ‘Potamides’ etruscum, from Italy.) It is possible and can also be found in shallow lagoons and saline lakes that the evolution of direct development in C. conica (or (Lozouet, 1986; Plaziat, 1993; Kowalke, 2001a). In Califor- its graeca-like ancestor) was linked to the environmental nia, Cerithideopsis californica occurs at high densities on crises (hypersalinity and cooling) in the Mediterranean intertidal mudflats and among saltmarsh plants (Race, during the Late Miocene. Whether this species maintained 1981); this species is predicted to be a member of the east- a continuous presence in the Mediterranean throughout ern Pacific Cerithideopsis clade (Houbrick, 1984; Fig. 2). the climatic fluctuations of the Pleistocene, or survived gla- These three species occupy terminal positions in the molec- cial intervals in an Indian Ocean refuge, is not known ular phylogeny (Fig. 2), so that their independence from (Lozouet, 1986). In either case, we agree with Lozouet mangroves is a derived condition. Parsimonious recon- (1986) that spread of C. conica to the Indian Ocean was struction of ancestral habitats therefore suggests that asso- recent, some time in the Quaternary, that it was facilitated ciation with mangroves is plesiomorphic within the entire by direct development and euryhalinity, and that transport radiation of living potamidids. The common ancestor of may have been effected by birds (see also Plaziat, 1993). Cerithideopsilla cingulata and C. conica is predicted to have The present distribution of C. cingulata is centred in the shared the same non-mangrove habitat, and was therefore western Pacific, but it is sympatric with C. conica in the able to colonize the Mediterranean in the Middle or Late northern Indian Ocean (e.g. Plaziat and Younis, 2005), Miocene, where mangroves were reduced to Avicennia where the two remain distinct. alone, and to survive the extinction of mangroves in the D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699 695

Mediterranean at the close of the Miocene (Plaziat et al., been used as mangrove indicators (Harzhauser, 2004; Rei- 2001). chenbacher et al., 2004; Dominici and Kowalke, 2007). The specialized tree-climbing habit is found in two pot- These ‘Tympanotonos’ have occasionally been found in amidid clades, Cerithidea (Houbrick, 1984; McGuiness, deposits with mangrove plant fossils and with Terebralia 1994; Ohtaki et al., 2002; Vannini et al., 2006) and Ceri- (Middle Eocene of Hungary, Kowalke, 2001b), but in other thideopsis (Keen, 1971; Plaziat, 1984; but not in all species, cases ‘Tympanotonos’andTerebralia occur in distinct facies e.g. Race, 1981; Houbrick, 1984). The shells show parallel (Kadolsky, 1988, 1995; Harzhauser and Kowalke, 2001). morphological adaptations of lightweight construction, At least some fossil ‘Tympanotonos’ are believed to have flared and planar apertures and (in Cerithidea) decollate inhabited shallow sublittoral, sandy, reef flats (Harzhauser, (shed) apices. Given the tree topology of Fig. 2, it is parsi- 2004). In the case of Vicarya (here considered a synonym of monious to reconstruct independent acquisition of tree- Potamides; Table 3) fossils may occur together with Tele- climbing in these two groups (but reconstruction would scopium and Terebralia, but it is not considered an indica- be equivocal under alternative resolutions of the basal tor of mangrove habitats (Oyama, 1950; Shimizu and polychotomy in Potamididae) from ground-dwelling ances- Kaneko, 1992; Taguchi, 1992, 2002). The acid soils of man- tors. This contrasts with the other tree-dwelling clade of groves are not conducive to preservation of molluscan mangrove-associated gastropods, the genus Littoraria, shells (Plaziat, 1995), so the abundance of Potamides which was derived from rock-dwelling ancestors (Reid, (and, indeed, of some Terebralia) in the fossil record argues 1999; Williams et al., 2003). There is a parallel among against a strict association with mangroves. At the least, tree-climbing crabs, of which the Sesarmidae had sedi- therefore, Potamides had a far wider range of habitats than ment-dwelling ancestors whereas Grapsidae were derived Recent potamidid genera, and the evidence for its associa- from rock-dwellers (Fratini et al., 2005). tion with mangroves is slight. Another extinct potamidid For fossil potamidids it is far more difficult to determine genus, Potamidopsis, is believed to have inhabited sandy their membership of mangrove ecosystems. Based on the sublittoral beds (Gitton et al., 1986,as‘Tympanot- ecology of their living species, some genera (Telescopium, onos trochlearis’) and lagoons of variable salinity (PL, Terebralia) have been used as indicators of fossil mangrove unpublished). assemblages (Oyama, 1950; Plaziat, 1995). For extinct spe- In conclusion, the molecular phylogeny in combination cies this argument is unsound unless confirmed by fossil with our survey of the fossil record, the ecology of Recent pollen or plant remains, and this evidence is seldom avail- and fossil potamidids, and the history of mangroves them- able. The three living species of Terebralia are closely asso- selves, suggests the following hypothesis. Diverse man- ciated with mangroves (with the exception noted above). grove forests first appeared in the Tethyan realm during During the Early and Middle Miocene, Terebralia bidenta- the Early Eocene (following a likely radiation in the Palae- ta was abundant in the Mediterranean and Paratethys, and ocene; Ellison et al., 1999; Plaziat et al., 2001). The living has been found with probable mangrove plant debris (Har- members of the Potamididae are a monophyletic radiation, zhauser and Kowalke, 2001) and Avicennia pollen (Plaziat, whose earliest certain representatives appeared in the Mid- 1995); however, it also extended beyond the likely northern dle Eocene of the Tethys (Fig. 2, Table 4). This historical limit of mangroves, so the association was not invariable and geographical coincidence of Recent mangrove and pot- (Plaziat, 1995; Plaziat et al., 2001). During the Late Oligo- amidid genera has been noted before (Glaubrecht, 1996, cene Terebralia rahti occurred in the Mainz Basin under 1997; Ellison et al., 1999; Kowalke, 2003). However, we semiarid conditions unfavourable for mangroves (Kadol- go further, and suggest that the living potamidids (subfam- sky, 1988); the same species was common during the Early ily Telescopiinae Allan, 1950) are a single adaptive radia- Miocene in the Aquitaine Basin in a lagoonal environment, tion that diversified in the new mangrove environment with no evidence of association with mangroves (PL, shortly after its appearance. The evolution of the potamid- unpublished). The Middle Eocene species Terebralia sub- ids has been intimately connected with that of the man- corvina has been found together with the remains of man- groves ever since, although a few species have lost this grove plants, as has Cerithideopsis vulcani (Kowalke, dependence (several species of Cerithideopsilla, Cerithide- 2001b). opsis, Terebralia, noted above). The detailed biogeographic In contrast, many fossil members of Potamides are history of potamidids is not yet understood, but at least believed to have inhabited shallow lagoons with low or var- some genera (Terebralia and Cerithideopsis) formerly had iable salinity (Lozouet, 1986; Kowalke, 2001a, 2006a; Har- a pantropical distribution and have become restricted (by zhauser and Kowalke, 2002) and even saline inland lakes extinction and vicariance, respectively), mirroring patterns (Plaziat, 1993; Kowalke, 2006b). (This palaeoecological in the mangrove genera, which in turn responded to global interpretation has been strengthened by comparison with climatic and tectonic events (Plaziat et al., 2001). The mod- Cerithideopsilla conica in similar habitats, and the belief ern pattern of potamidid diversity, with a focus in the cen- that it is the surviving representative of Potamides, but this tral Indo-West Pacific, matches that of mangrove species is refuted above.) The larger members of Potamides have (Ellison et al., 1999; Ellison, 2002). Only those potamidids frequently been identified as ‘Tympanotonos’ and, by anal- that have lost their association with mangroves (e.g. Cerith- ogy with the Recent mangrove-associated T. fuscatus, have ideopsilla conica) have been able to colonize temperate 696 D.G. Reid et al. / Molecular Phylogenetics and Evolution 47 (2008) 680–699 coastlines where mangroves do not occur. Vegetated salt- Bandel, K., 2006. Families of the Cerithioidea and related superfamilies marsh habitats existed before the appearance of the distinc- (Palaeo-; ) from the to the Recent tive mangrove environment (Plaziat et al., 2001), and may characterized by protoconch morphology—including the description of new taxa. Freiberger Forschungshefte C511, 59–138. have been inhabited by extinct potamidid genera (Bandel Bandel, K., Kowalke, T., 1999. Gastropod fauna of the Cameroonian and Riedel, 1994; Kowalke and Bandel, 1996; Kowalke, coasts. 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