Left in the cold? Evolutionary origin of Laternula elliptica, a keystone bivalve species of Antarctic benthos

Left in the cold? Evolutionary origin of Laternula elliptica, a keystone bivalve species of... Abstract The large, burrowing bivalve Laternula elliptica is an abundant component of shallow-water soft-substrate communities around Antarctica but its congeners are temperate and tropical in distribution and their phylogenetic relationships are obscure. A new molecular analysis of Laternulidae species shows that there are two distinct clades, one of Exolaternula species, E. spengleri and E. liautaudi, possessing a ligamental lithodesma and a larger clade of species lacking the lithodesma. Of the latter, Laternula elliptica is a sister taxon to temperate and tropical species, including those that live around the coasts of Australia from Tasmania to Darwin. It is suggested that L. elliptica was left isolated around Antarctica following the opening of the Tasman Gateway and initiation of the Circum-Antarctic Current as Australia drifted northwards following the final breakup of Gondwana. A further scenario is that as Australia moved closer to Asia, species spread into tropical habitats and more widely to the Red Sea and Japan. Exolaternula species have a likely Tethyan origin and the present-day range is from the Arabian Gulf, around southern Asia and as far north as southern Russia. INTRODUCTION Although the precise origins of the modern Antarctic marine fauna are undoubtedly complex, there has always been a distinct impression that certain elements within it are both of considerable antiquity and endemic to the southern high latitudes (Lipps & Hickman, 1982; Clarke & Crame, 1989). In all probability these taxa date back to at least the Late Cretaceous – Early Palaeogene, a time when the southern margins of the Gondwana supercontinent were still more or less intact, and polar climates were significantly warmer than those of today. Zinsmeister’s (1982) extensive shallow marine Weddellian Province, stretching from southern Patagonia through western Antarctica to New Zealand and eastern Australia, was established on the basis of various endemic molluscan families, one of which, the Struthiolariidae (Littorinimorpha; Stromboidea), still occurs in the region (Beu, 2009). As our knowledge of both the fossil record and the molecular phylogenetics of Antarctic marine taxa has steadily improved, it is becoming appropriate to ask how certain specific elements within the fauna may have evolved. Do their roots lie in some form of ancestral Weddellian province, or were they more recent immigrants? This sort of question is particularly apposite for the very common infaunal bivalve Laternula elliptica (Anomalodesmata; Laternulidae), as its congeners can be traced northwards through temperate South Australia into the heart of the tropical Indo-Pacific realm, and then northwards again into the temperate North-West Pacific. Is this a genus that spread either into or out of Antarctica, and if so, when? Laternula elliptica (King, 1832) is a large (> 100 mm) infaunal bivalve abundant in shallow water and even intertidal habitats around the Antarctic continent and sub-Antarctic islands (Fig. 1A–C). Its abundance and prominence in benthic communities, and its rank as a keystone species by Harper et al. (2012), has attracted considerable research interest with a multitude of publications investigating many aspects of its biology and ecology. A few examples include: physiology (Morley et al., 2009, 2012), biochemistry (González & Puntarulo, 2011), reproduction (Kang, Ahn & Choi, 2003), growth rates (Ralph & Maxwell, 1977; Brey et al., 2011), burrowing behaviour (Peck et al., 2009), trace metals (Ahn et al., 1996), shell microstructure and mineralogy (Sato-Okoshi & Okoshi, 2008; Nehrke et al., 2012), ice scour damage (Harper et al., 2012) and proteomics (Clark et al., 2010). Figure 1. View largeDownload slide Laternula elliptica, type species of Exolaternula and Laternula, and fossil Laternulidae. A. Laternula elliptica (King, 1832), James Ross Island, Antarctica (NHMUK), L = 69 mm. B, C. Laternula elliptica, in life position with fused inhalant and exhalant siphons. Images by David Cothran/Lindblad Expeditions, All Rights Reserved. D. Exolaternula spengleri (Gmelin, 1792) (senior synonym of A. truncata, A. rostrata), Port Essington, Australia (NHMUK), L = 78.4 mm. E. Laternula anatina (Linnaeus, 1758), Moluccas (NHMUK), L = 55.2 mm. F. Laternula elliptica, Early Pliocene, Cockburn Island Formation, Cockburn Island, north-eastern Antarctic Peninsula (BAS DJ. 351.21), L = 138 mm. G. Laternula burdigalensis (Cossmann & Peyrot, 1909), Miocene, Salles, France, L = 80 mm (from Cossmann & Peyrot, 1909). H, I. Laternula. sp., Eocene, Rio Turbio Formation, Patagonia, Argentina, L = 50 mm, from Griffin (1991) with permission Journal of Paleontology. Figure 1. View largeDownload slide Laternula elliptica, type species of Exolaternula and Laternula, and fossil Laternulidae. A. Laternula elliptica (King, 1832), James Ross Island, Antarctica (NHMUK), L = 69 mm. B, C. Laternula elliptica, in life position with fused inhalant and exhalant siphons. Images by David Cothran/Lindblad Expeditions, All Rights Reserved. D. Exolaternula spengleri (Gmelin, 1792) (senior synonym of A. truncata, A. rostrata), Port Essington, Australia (NHMUK), L = 78.4 mm. E. Laternula anatina (Linnaeus, 1758), Moluccas (NHMUK), L = 55.2 mm. F. Laternula elliptica, Early Pliocene, Cockburn Island Formation, Cockburn Island, north-eastern Antarctic Peninsula (BAS DJ. 351.21), L = 138 mm. G. Laternula burdigalensis (Cossmann & Peyrot, 1909), Miocene, Salles, France, L = 80 mm (from Cossmann & Peyrot, 1909). H, I. Laternula. sp., Eocene, Rio Turbio Formation, Patagonia, Argentina, L = 50 mm, from Griffin (1991) with permission Journal of Paleontology. Outside of the Southern Ocean, Laternula species range from the southern temperate zone (Tasmania) through subtropical and tropical Australia, south-eastern Asia, Philippines, China and Japan as far north as Peter the Great Bay in western Russia; and to the west through the northern Indian Ocean, Arabian Gulf, Red Sea and, rarely, to East Africa, but they are absent from oceanic islands. One species, L. liautaudi, is exotic to west coast USA (Miller, Coan & Chapman, 1999 as L. marilina; or L. gracilisFofonoff et al., 2017) and another, L. anatina, to the eastern Mediterranean (Gofas & Zenetos, 2003). The genus is particularly speciose around Australia from where 12 nominal species have been described or recorded. By contrast to the research focus on L. elliptica, there are relatively few studies devoted to the temperate and tropical species of Laternula and most aspects of their biology and systematics remain uninvestigated. Exceptions are the morphological and ecological studies of Laternula rostrata by Morton (1973, 1976), Adal & Morton (1973) and Prezant et al. (2008), the physiology of species from Singapore and South Australia (Morley et al., 2009; Lai et al., 2011) and China (Zhuang, 2005), and ecological studies on Korean and Japanese species (Kang et al., 2006; Kanaya, Takagi & Kikuchi, 2008). Laternula species have thin, elongate, nacreous and granular prismatic shells, a posterior gape and an external surface covered in short spikes (Checa & Harper, 2010). There is a prominent umbonal slit in the shell with an internal shell buttress posterior to the hinge (Savazzi, 1990). The internal ligament is set on a chondrophore, and an anterior, transverse lithodesma (a calcified ossicle within the ligament) is present in some species. Siphons are long, fused and periostracum-covered (Fig. 1), with distal tentacles and siphonal eyes (Morton, 1973; Adal & Morton, 1973). The ventral mantle is fused, with a small pedal gape, and the foot is small. Arenophilic mantle glands are present on siphons (Sartori, Passos & Domaneschi, 2006) and their sand adherent secretions are present on juvenile shells < 10 mm long (E. M. Harper, unpub. obs). Laternulids live in muddy, intertidal or shallow subtidal habitats, often amongst or near mangroves (Prezant et al., 2008; Lai et al., 2011), in seagrass beds (our personal observations) and frequently in habitats of fluctuating or elevated salinities. Compared with its lower latitude congeners, Laternula elliptica is larger, thicker shelled (Watson et al., 2012; Prezant, Shell & Wu, 2015) and lacks the spikes (spinules) on the shell surface present in all other species. Apart from L. elliptica, discrimination of Laternula species is extremely confused and misidentifications abound. There is no real agreement on the number of living species; the latest taxonomic account (Huber, 2010) recognized 19 species (20 species in WoRMS, 2017), while previously Lamy (1934) documented 15–20 species and in the best illustrated of the 19th century monographs Reeve (1860–1863) illustrated 30 species with 24 of these described as new. The type specimens from Reeve (NHMUK) are a major resource for any taxonomic study of the genus. We agree with Huber (2010) that species depictions and distributional data in many identification guides (e.g. Lamprell & Healy, 1998) and other publications (Morton, 1976) are wrongly assigned and have led to continuing confusion. Laternula species have been divided into two subgenera (Habe, 1977) on the basis of the presence (Exolaternula) or absence (Laternula) of a lithodesma. Nevertheless, the taxonomic or phylogenetic significance of this character has been doubted (Huber, 2010). In a broader context, molecular analyses (Harper, Dreyer & Steiner, 2006; Combosch et al., 2017; Williams et al., 2017) place Laternula within the Anomalodesmata in a clade with Lyonsiidae, Clavagellidae and Pandoridae but distinct from Cochlodesma (Periplomatidae) which has a similar umbonal slit but which groups with Thraciidae and Myochamidae. Clearly, L. elliptica is a prominent and ecologically important element in Antarctic benthic faunas but is biogeographically isolated from the warmer water species of the genus. In this study we use a molecular analysis to investigate the phylogenetic relationships of L. elliptica to the lower latitude species and evaluate three possible biogeographical scenarios concerning its present isolation in polar seas. Is L. elliptica a relict species dating from a former, broader, distributional range of the genus and warmer Antarctic conditions (e.g. during the Early–Middle Eocene) but now isolated by the formation of the Circum-Antarctic Current and has subsequently become physiologically adapted to cold conditions? An expectation arising from this scenario might be that L. elliptica is most closely related to the temperate southern Australian species. Another possibility is that Laternula species originated on Late Gondwanan shallow shores and rafted northwards with Australia into the tropics after the split from Antarctica c. 30 Mya, leaving L. elliptica isolated in the Southern Ocean. This may account for the diversity of Laternula species around Australia from temperate conditions around Victoria/Tasmania to tropical waters to the north. Laternula species then spread and diversified into tropical Asian shallow-water environments. An expectation would be that L. elliptica is sister to all other species or groups with the Australian taxa. A further scenario that matches the ‘out of the tropics’ (OTT) model developed by Jablonski, Roy & Valentine (2006) and Jablonski et al. (2013) is that Laternula diversified on tropical–subtropical shores and later spread southwards into Antarctica during warmer periods, with L. elliptica as a derived species. MATERIAL AND METHODS Molecular methods The DNA extraction and amplification protocols of Williams et al. (2013) were used to amplify portions of four genes from 16 specimens (Table 1). The genes amplified were the nuclear 28S rRNA gene (approximately 1640 bp) and three mitochondrial genes: 12S rRNA gene (approximately 610 bp), 16S rRNA gene (approximately 500 bp) and cytochrome b (405 bp). Lyonsia norwegica (Lyonsiidae) and Bryopa lata (Clavagellidae) were used as outgroups having been shown in previous analyses to be sister groups of Laternulidae (Harper et al., 2006; Combosch et al., 2017; Williams et al., 2017). Sequence reactions were performed directly on purified PCR products using the BigDye Terminator v1.1 Cycle Sequencing Kit (Applied Biosystems) and run on an Applied Biosystems 3730 DNA Analyzer automated capillary sequencer. Sequences for each gene fragment were assembled and edited using Sequencher (v.5.1; Gene Codes Corporation). Table 1. Laternulidae species included in the analysis with collection localities, locality codes used in Figure 2, museum registration numbers for vouchers and GenBank accession numbers for the genes sequenced for each taxon   Collection locality  Locality code  Voucher number  28S  cyt B  12S  16S  Exolaternula liautaudi (Mittre, 1844)  Olga Bay, Eastern Russia, 43°41′56″N, 135°15′04″E  OB 1  NHMUK 20170326  LT960470  LT960693  LT960373  LT960384  Exolaternula liautaudi (Mittre, 1844)  Olga Bay, Eastern Russia, 43°41′56″N, 135°15′04″E  OB 2  NHMUK 20170327  LT960471  LT960694  LT960374  LT960385  Exolaternula liautaudi (Mittre, 1844)  Kojima-Shinden, Kawasaki, Japan, 35°30′52″N, 139°48′29″E  KS  NHMUK 20170328  LT960472  LT960695    LT960386  Exolaternula spengleri (Gmelin, 1792)  Casiguran Bay, Luzon, Philippines, 16°15.95′N, 122°05′E  LP  MNHN IM-2007-41446  LT960473      LT960387  Exolaternula spengleri (Gmelin, 1792)  Sungei Buroh, Singapore, 1°26′39″N, 103°43′39″E  SIN  NHMUK 20160581  LT960474  KX815963  KX815963  KX815967  Laternula elliptica (King, 1832)  Rothera Point, Adelaide Island, Antarctica, 67°34′S, 68°08′W  RO  no voucher  LT960475  KX815959  KX815959  KX815959  Laternula elliptica (King, 1832)  King George Island, South Shetland Islands, 62°09.87′S, 58°33.83′W  SS  NHMUK 20170329  LT960476  LT960696    LT960388  Laternula creccina (Reeve, 1860)  Esperance, Bandy Creek, W. Australia, 33°49′50″S, 121°56′10″E  ESP  NHMUK 20030177  LT960477  LT960697    LT960389  Laternula anatina (Linnaeus, 1758)  Papua New Guinea, near Rempi, stn PR104, 5°5′6″ S,145°48′E  PNG  MNHN IM-2013-15152  LT960478  LT960698  LT960375  LT960390  Laternula japonica (Lischke, 1872)  Hakata-jima Island, Ehime pref., Japan, 34°12′N, 133°05′E  HJ  NHMUK 20170330  LT960479    LT960376  LT960391  Laternula cf. boschasina (Reeve, 1860)  Ludmilla Creek, Darwin, Australia, 12°24′28″S, 130°50′07″E  DAR  NHMUK 20170331  LT960480  LT960699  LT960377    Laternula cf. bullata (Reeve, 1860)  Sungei Buroh, Singapore; 1°26′39″′N, 103°43′39″E  SIN  NHMUK 20170332  LT960481  LT960700  LT960378  LT960392  Laternula sp.  Kungkraben Bay, Thailand, 12°34.42′N, 101°54.24′E  KK  NHMUK 20170333  LT960482  LT960701  LT960379  LT960393  Laternula cf. corrugata (Reeve, 1863)  Denham, Shark Bay, W. Australia, 25°54′11″S, 118°31′16″E  SB  NHMUK 20170334  LT960483  LT960702  LT960380  LT960394  Laternula gracilis (Reeve, 1860)  Geelong, Victoria, Australia, 38°9′07″S, 144°23′44″E  GE 1  NHMUK 20170335    LT960703  LT960381  LT960395  Laternula gracilis (Reeve, 1860)  Geelong, Victoria, Australia, 38°9′07″S, 144°23′44″E  GE 2  NHMUK 20170336  LT960484    LT960382  LT960396  Laternula gracilis (Reeve, 1860)  Burrill Lake, NSW, Australia, 35°22′03″S, 150°26′04″E  BL  NHMUK 20170337  LT960485  LT960704  LT960383  LT960397  Laternula gracilis (as L. marilina in Taylor et al., 2007)  N. Stradbroke Island, Moreton Bay, Qld, Australia, 27°24′29″S, 153°24′42″E  MB 1  NHMUK 29970221  AM779661        Laternula gracilis (Reeve, 1860)  N. Stradbroke Island, Moreton Bay, Queensland, Australia  MB 2  Combosch et al., (2017)  KX713395      KX713227  Outgroups  Bryopa lata (Broderip, 1834)  Singapore, 1°13.9′N, 103°52′E    NHMUK 20160581  LT960486  KX815957  KX815957  KX815957  Lyonsia norwegica (Gmelin, 1792)  Tjärno, Sweden, 58°52.42′N, 11°06.18′E    NHMUK 20160584  LT960487  KX815960  KX815960  KX815960    Collection locality  Locality code  Voucher number  28S  cyt B  12S  16S  Exolaternula liautaudi (Mittre, 1844)  Olga Bay, Eastern Russia, 43°41′56″N, 135°15′04″E  OB 1  NHMUK 20170326  LT960470  LT960693  LT960373  LT960384  Exolaternula liautaudi (Mittre, 1844)  Olga Bay, Eastern Russia, 43°41′56″N, 135°15′04″E  OB 2  NHMUK 20170327  LT960471  LT960694  LT960374  LT960385  Exolaternula liautaudi (Mittre, 1844)  Kojima-Shinden, Kawasaki, Japan, 35°30′52″N, 139°48′29″E  KS  NHMUK 20170328  LT960472  LT960695    LT960386  Exolaternula spengleri (Gmelin, 1792)  Casiguran Bay, Luzon, Philippines, 16°15.95′N, 122°05′E  LP  MNHN IM-2007-41446  LT960473      LT960387  Exolaternula spengleri (Gmelin, 1792)  Sungei Buroh, Singapore, 1°26′39″N, 103°43′39″E  SIN  NHMUK 20160581  LT960474  KX815963  KX815963  KX815967  Laternula elliptica (King, 1832)  Rothera Point, Adelaide Island, Antarctica, 67°34′S, 68°08′W  RO  no voucher  LT960475  KX815959  KX815959  KX815959  Laternula elliptica (King, 1832)  King George Island, South Shetland Islands, 62°09.87′S, 58°33.83′W  SS  NHMUK 20170329  LT960476  LT960696    LT960388  Laternula creccina (Reeve, 1860)  Esperance, Bandy Creek, W. Australia, 33°49′50″S, 121°56′10″E  ESP  NHMUK 20030177  LT960477  LT960697    LT960389  Laternula anatina (Linnaeus, 1758)  Papua New Guinea, near Rempi, stn PR104, 5°5′6″ S,145°48′E  PNG  MNHN IM-2013-15152  LT960478  LT960698  LT960375  LT960390  Laternula japonica (Lischke, 1872)  Hakata-jima Island, Ehime pref., Japan, 34°12′N, 133°05′E  HJ  NHMUK 20170330  LT960479    LT960376  LT960391  Laternula cf. boschasina (Reeve, 1860)  Ludmilla Creek, Darwin, Australia, 12°24′28″S, 130°50′07″E  DAR  NHMUK 20170331  LT960480  LT960699  LT960377    Laternula cf. bullata (Reeve, 1860)  Sungei Buroh, Singapore; 1°26′39″′N, 103°43′39″E  SIN  NHMUK 20170332  LT960481  LT960700  LT960378  LT960392  Laternula sp.  Kungkraben Bay, Thailand, 12°34.42′N, 101°54.24′E  KK  NHMUK 20170333  LT960482  LT960701  LT960379  LT960393  Laternula cf. corrugata (Reeve, 1863)  Denham, Shark Bay, W. Australia, 25°54′11″S, 118°31′16″E  SB  NHMUK 20170334  LT960483  LT960702  LT960380  LT960394  Laternula gracilis (Reeve, 1860)  Geelong, Victoria, Australia, 38°9′07″S, 144°23′44″E  GE 1  NHMUK 20170335    LT960703  LT960381  LT960395  Laternula gracilis (Reeve, 1860)  Geelong, Victoria, Australia, 38°9′07″S, 144°23′44″E  GE 2  NHMUK 20170336  LT960484    LT960382  LT960396  Laternula gracilis (Reeve, 1860)  Burrill Lake, NSW, Australia, 35°22′03″S, 150°26′04″E  BL  NHMUK 20170337  LT960485  LT960704  LT960383  LT960397  Laternula gracilis (as L. marilina in Taylor et al., 2007)  N. Stradbroke Island, Moreton Bay, Qld, Australia, 27°24′29″S, 153°24′42″E  MB 1  NHMUK 29970221  AM779661        Laternula gracilis (Reeve, 1860)  N. Stradbroke Island, Moreton Bay, Queensland, Australia  MB 2  Combosch et al., (2017)  KX713395      KX713227  Outgroups  Bryopa lata (Broderip, 1834)  Singapore, 1°13.9′N, 103°52′E    NHMUK 20160581  LT960486  KX815957  KX815957  KX815957  Lyonsia norwegica (Gmelin, 1792)  Tjärno, Sweden, 58°52.42′N, 11°06.18′E    NHMUK 20160584  LT960487  KX815960  KX815960  KX815960  MNHN, Muséum national dHistoire Naturelle, Paris; NHMUK, The Natural History Museum, London. View Large Figure 2. View largeDownload slide Combined gene tree for Laternulidae based on sequences from four genes (28S rRNA, 12S, 16S and cyt b) using Bayesian inference as implemented by MrBayes. Support values are posterior probabilities (PP). Images are of sequenced specimens or proxies – not to scale. Colour code on localities denotes: tropical (red), temperate (green) and Antarctic (blue) Locality codes used on the tree: BL – Burrill Lake, New South Wales, Australia; DAR – Darwin, Australia; ESP – Esperance, Western Australia; HJ – Higata-Jima Island, Japan; GE – Geelong, Victoria, Australia; KK – Kungkraben Bay, Thailand; KS – Kojima-Shinden, Japan; LP – Luzon, Philippines; MB – Moreton Bay, Queensland, Australia; OB – Olga Bay, eastern Russia; PNG – Papua New Guinea; RO – Rothera, Adelaide Island, Antarctica; SB – Shark Bay, Western Australia; SIN – Singapore; SS – South Shetland Islands. Figure 2. View largeDownload slide Combined gene tree for Laternulidae based on sequences from four genes (28S rRNA, 12S, 16S and cyt b) using Bayesian inference as implemented by MrBayes. Support values are posterior probabilities (PP). Images are of sequenced specimens or proxies – not to scale. Colour code on localities denotes: tropical (red), temperate (green) and Antarctic (blue) Locality codes used on the tree: BL – Burrill Lake, New South Wales, Australia; DAR – Darwin, Australia; ESP – Esperance, Western Australia; HJ – Higata-Jima Island, Japan; GE – Geelong, Victoria, Australia; KK – Kungkraben Bay, Thailand; KS – Kojima-Shinden, Japan; LP – Luzon, Philippines; MB – Moreton Bay, Queensland, Australia; OB – Olga Bay, eastern Russia; PNG – Papua New Guinea; RO – Rothera, Adelaide Island, Antarctica; SB – Shark Bay, Western Australia; SIN – Singapore; SS – South Shetland Islands. Mitochondrial genes of another four taxa, Lyonsia norwegica, Bryopa lata, Laternula elliptica (Antarctica) and Laternula rostrata (Singapore, herein E. spengleri), were previously published as complete, or nearly complete, mitochondrial genomes (Williams et al., 2017) and 12S, 16S and cytB sequence data were taken from these sequences (GenBank accession numbers KX815957, KX815959, KX815960 and KX815963). Sequences for 28S rRNA genes were obtained from the same NGS genomic data set used in Williams et al. (2017) to assemble mitochondrial genomes. Briefly, genomic DNA was sequenced on one-fifth of a flowcell on an Illumina MiSeq platform (v.2 chemistry; 2 × 250 paired-end). Reads were analysed and assembled using Geneious (v.8.1.8; https://www.geneious.com). The data were trimmed allowing no ambiguous base calls and removing bases from the terminal ends of reads with an error probability of 0.05 or higher (i.e. those with a greater than 5% chance of being incorrect). The trimmed reads were first assembled de novo and the resulting contigs were interrogated against the NCBI database, using BLAST (Altschul et al. 1990), in order to identify ribosomal gene sequences. Gene boundaries were determined by comparison with other molluscan taxa. Coverage data are available in Williams et al. (2017). Phylogenetic datasets analysed included three individual gene datasets and a combined gene dataset including all individuals that had sequences for at least three genes. Alignment of cytB sequences was unambiguous and no stop codons were observed. Sequences of ribosomal genes were aligned in Geneious (v.8.1.8) using ClustalW. Poorly aligned sites in the ribosomal gene alignments were identified using the online Gblock server using all three options for a less stringent selection (v.0.91b; Castresana, 2000, http://molevol.cmima.csic.es/castresana/Gblocks_server.html) and removed from alignments. After removal of ambiguously aligned blocks of data, a total of 2922 bp of aligned sequence remained to be used in phylogenetic analyses for the combined gene dataset (90% of the original 3241positions). In individual analyses, alignment lengths after Gblocks were 444 bp of sequence from 16S rRNA (89% of 495 bp in the original alignment), 539 bp of 12S rRNA (90% of 597 bp in the original alignment) and 1575 bp of 28S rRNA (88% of 1785 bp in the original alignment). The best nucleotide substitution models were determined using jModelTest (v.X; Darriba et al. 2012) using the Akaike information criterion (AIC). The best nucleotide substitution models were for cytB HKY+I+G and for all three rRNA genes GTR+I+G. These models were used in Bayesian phylogenies implemented in MrBayes (v.3.2.6; Huelsenbeck & Ronquist, 2001). The analysis ran for 10000000 generations, with a sample frequency of 1000. The first 10% were discarded as burn-in after checking that runs had reached stationarity. Stationarity was determined by examining traces in TRACER (v.1.6 http://tree.bio.ed.ac.uk/software/tracer/). Convergence between the two runs was tested by examining traces using TRACER and by checking that the potential scale reduction factors produced by the ‘sump’ command in MrBayes were close to one (Gelman & Rubin, 1992) and that the mean standard deviation of split frequencies approached zero. Taxonomic rationale Because the species taxonomy of Laternula is so confused, care was taken to identify the taxa included in the molecular analyses. Type material of Laternula species was examined in NHMUK and MNHN along with images of other relevant specimens from ANSP, NHMD, MHNG and WAM. Using these, plus the taxonomic revisions of Reeve (1860), Lamy (1934) and most recently Huber (2010) and figures in regional faunas (e.g. Lamprell & Healy, 1998; Okutani, 2000; Lutaenko & Noseworthy, 2012) augmented by the results of our molecular analysis herein, we have derived an outline taxonomic classification (Appendix) listing what we believe are extant species and their synonyms. Notable taxonomic changes resulting from study of type material (NHMD) are that Solen spengleriGmelin, 1792 (herein Exolaternula spengleriFig. 1D) is an earlier name for the species variously called L. anserifera (Spengler, 1793), L. truncata (Lamarck, 1818 auct.) or L. rostrata (Sowerby, 1839). Images of newly separated valves of the holotype of Anatina liautaudiMittre, 1844 (MNHN IM–2000–33234) indicate that it is the earliest name (herein as Exolaternula liautaudi) for the variously named north-east Asian margin species. Also, genetic data (herein) show that the Australian species variously identified as Laternula gracilis, L. marilina and L. recta are a single species, with L. gracilis (Reeve, 1860) having priority. Our present estimate is that there are 15 living species of Laternulidae; further and more comprehensive sampling will probably resolve some problem areas but may also reveal the existence of cryptic species. Institutional abbreviations: ANSP, Academy of Natural Sciences Philadelphia at Drexel University, USA; BAS, British Antarctic Survey, Cambridge, UK; MAGNT, Museum and Gallery of Northern Territory, Australia; MHNG, Muséum d’histoire naturelle, Geneva, Switzerland; MNHN, Muséum national d’Histoire naturelle, Paris, France; NHMD, Natural History Museum of Denmark, Copenhagen; NHMUK, The Natural History Museum, London, UK; WAM, Western Australian Museum, Perth, WA. RESULTS All individual gene trees had similar topologies to each other and to the combined gene tree shown in Figure 2. A clear result is that the sequenced Laternulidae species split into two major groups, one comprising L. spengleri from Singapore and Philippines and L. liautaudi from Japan and south-eastern Russia and a second, larger group containing all the other species including L. elliptica. A robust topology in all gene trees is that, in the larger clade, Laternula elliptica is the sister group, with maximum support (P = 1.0), to all the other Laternula species from Australia, south-eastern Asia and southern Japan. Amongst the temperate and tropical samples are three well-supported sub-clades. One consists of three Laternula collected from near Esperance (southern Western Australia), Papua New Guinea and southern Japan; these are similar to Laternula anatina in shell form but are genetically different from each other and we have identified them as L. creccina, L. anatina and L. japonica. The cooler water Laternula creccina is the sister group to the two warm water species. A second sub-clade includes three samples collected at Darwin, Singapore and eastern Thailand but differ from each other in the molecular tree. The sample from Darwin is closest in shell characters to L. boschasina. The specimen from Singapore resembles the syntypes of L. bullata and differs from the Kungkraben Bay, Thailand, example which we retain as Laternula sp. The third sub-clade comprises Laternula from southern and eastern Australia [Port Phillip Bay (Victoria), Burrill Lake (New South Wales) and Moreton Bay (Queensland)]. Laternula from these locations have been variously named in collections as L. gracilis, L. recta and L. marilina but these have only minor genetic differences, suggesting that they are conspecific, with L. gracilis having taxonomic priority. A species from Shark Bay, Western Australia, that we identify as L. cf. corrugata, is a sister to the eastern Australian Laternula gracilis. Geological record of Laternula Other anomalodesmatans possessing an umbonal slit (Periplomatidae) have been confused with Laternula, especially in fossils, and many records of fossil Laternula can be discounted. For example, the so-called Laternula fuchsi (Hoernes, 1875) widely reported from the Miocene (Burdigalian) of eastern Europe (Harzhauser, Mandic & Schlögl, 2011) is a periplomatid, as is Laternula ravniSchnetler, 2001 from the Palaeocene of Denmark. Furthermore, the ‘Laternula’ species widely reported from the Cenozoic of far Eastern Russia are now classified as Periplomatidae (Kafanov, Ogasawara & Marincovich, 2001). A search of the fossil literature for records of bivalves that resemble our concept of Laternula indicates that they are rare. This may be a consequence of the poor preservation potential of the thin, fragile, aragonitic shells and also the association with mangrove and organic-rich sediments from estuarine settings. Anatina burdigalensisCossmann & Peyrot, 1909 (122-3 pl. LXIII fig. 34) from the Miocene (Serravallian 13.82–11.63 Mya) of the Aquitaine Basin, France, resembles the living Exolaternula spengleri in shape (Fig. 1G). Fossils resembling the living Exolaternula liautaudi have been recorded as L. limicola from the mid-Miocene of central Japan (Itoigawa et al., 1981, 1982). Crame (1984) reported Laternula spp. from late Neogene (Pliocene?) deposits of the Makran coast, Pakistan, and these samples (in NHMUK) have shapes resembling living L. anatina. An earlier fossil from the Eocene Rio Turbio Formation of Patagonia [mid-Lutetian to mid-Priabonian, 44.6–34 Mya, date from González Estebenet et al. (2014)], described and figured as Laternula sp. by Griffin (1991: fig. 10 1-2), is broadly similar to L. spengleri in shape (Fig. 1H, I). A possible Late Cretaceous (Campanian/Maastrichtian) Laternula sp. has been described from Argentina (Parras & Griffin, 2013); this is more equivocal in attribution but has an umbonal slit and buttress. Further back in time some Mesozoic genera have been assigned to the Laternulidae, namely Anatimya, Cercomya, Plectomya and Platymyoidea (Keen & Cox, 1969) but these appear morphologically distant from living Laternula. History of Laternula in Antarctica Careful re-examination of both reference collections and the literature indicates that there are no bona fide Early Cenozoic representatives of Laternula from the extensive Early Cenozoic fossil record of Antarctica. The Oligocene–Miocene interval is much less complete (Beu, 2009; Beu & Taviani, 2014). The earliest unequivocal record of the genus is that known from the Cockburn Island Formation, which forms part of a complex sequence of glacial and interglacial sediments interbedded with the late Neogene James Ross Island Volcanic Group (JRIVG), north-eastern Antarctic Peveninsula (Smellie, Johnson & Nelson, 2013; Beu & Taviani, 2014). Specimens from the type area of the formation, Cockburn Island (64°12′S, 56°50′W), were assigned to Laternula elliptica by both Soot-Ryen (1952) and Jonkers (1998a), with the only difference being that their maximum size (150 mm+ in length) somewhat exceeded those of the modern form (Fig. 1F). However, in all other respects they are very close to living L. elliptica and we see no need to assign them to a separate taxon. Co-occurring specimens of the large pectinid Austrochlamys anderssoni (Hennig) have been reliably dated at 4.7 Mya by 87Sr/86Sr isotopes, and this age agrees well with that of 4.7–4.9 Mya for underlying basaltic lavas of the JRIVG (40Ar/39Ar dating) (Smellie et al., 2013). The 4.7 Mya age (i.e. earliest Pliocene) for the specimens of L. elliptica from Cockburn Island represents the earliest definitive fossil record of the genus from Antarctica. Within the James Ross Island group there are sparse records of Laternula from younger glacial/interglacial sediments interbedded with the JRIVG (i.e. the Hobbs Glacier Formation and its lateral equivalents). For example, Laternula sp. is noted from the southern end of Sykes Cliffs on the western side of Croft Bay (64°01′S, 57°49′W) (Jonkers, 1998b), and a poorly constrained 40Ar/39Ar age from overlying lavas was resolved to be 2.38 Mya (Smellie et al., 2013). A potentially older Antarctic specimen of Laternula has been recovered from the Battye Glacier Formation, Prince Charles Mountains, East Antarctica (70°48′S, 68°20′E). Although it clearly possesses a buttressed chondrophore and nacreous inner shell layer, it is very incomplete and can only doubtfully be referred to Laternula? sp. (Stilwell, Harwood & Whitehead, 2002: fig. 2m, n). The suggested Middle–Late Miocene age range for the Battye Glacier Formation is based on the associated diatom assemblage. Better preserved material is available from the Sørsdal Formation, Marine Plain, Vestfold Hills, East Antarctica (68°38′S, 78°8′E), and this has been identified as L. elliptica (Quilty et al., 2016). The Sørsdal Formation is dated by diatoms as Early Pliocene, 4.2–4.1 Mya (Quilty et al., 2016). There is an Early Pleistocene (Galasian) record of L. elliptica from the Scallop Hill Formation of McMurdo Sound (78°11′S, 166°58′E) (Speden, 1962; Beu & Taviani, 2014), and widespread evidence for a Late Quaternary to Holocene circum-Antarctic distribution of the species (Pickard, 1985). DISCUSSION The results show clearly that there are two distinct phylogenetic groups of Laternula species: the clade comprising L. spengleri and L. liautaudi with both species possessing a lithodesma, and the larger clade of all the other species where it is lacking in the adult. A lithodesma is present in the majority of anomalodesmatan families including Pandoridae, Lyonsiidae and Clavagellidae, the sister clades to Laternula (Harper, Hide & Morton, 2000; Harper et al., 2006). Thus, its presence in some species is interpreted as a retained plesiomorphic character and its absence in the larger clade as an apomorphic state. Contrary to Savazzi (1990: 100), only three species of Laternula are known to possess a lithodesma in adult shells: L. spengleri, L. liautaudi and L. erythraea (the last not molecularly sampled). Laternula spengleri and L. liautaudi form a robust clade that supports their classification in a distinct genus, Exolaternula, although other shell characters appear similar to Laternula species. Significantly, Sartori (2009) reported and illustrated lithodesmas in juvenile L. elliptica with shell lengths less than c. 12 mm but these become resorbed in larger shells. This ontogenetic loss of a lithodesma has also been reported in some Thraciidae species (Sartori & Ball, 2009). The three known Exolaternula species are distributed today (Fig. 3) along the northern Indian Ocean and Arabian Gulf (E. erythraea), through south-east Asia (E. spengleri), China, Korea and Japan as far north as Peter the Great Bay, Russia (E. liautaudi). Exolaternula liautaudi also occurs as an exotic on the west coast of the USA (Miller et al., 1999). The distribution of E. spengleri touches the very north of Australia, with a single 19th century (NHMUK) record from Port Essington, Northern Territory. The distribution given in Lamprell & Healy (1998) of this species (as L. rostrata) around southern Australia and New South Wales and followed in some ecological studies is erroneous and based on misidentifications. Figure 3. View largeDownload slide Distributional ranges of Exolaternula and Laternula species in the Indo-West Pacific and Southern Oceans. Robinson projection. Red – Exolaternula, blue – Laternula, green – Laternula elliptica. Figure 3. View largeDownload slide Distributional ranges of Exolaternula and Laternula species in the Indo-West Pacific and Southern Oceans. Robinson projection. Red – Exolaternula, blue – Laternula, green – Laternula elliptica. It seems likely that Exolaternula split from the other Laternula in the early Cenozoic with the clade having a different biogeographical history. We suggest that the present distribution of Exolaternula, restricted to the northern Indian Ocean and southern and eastern margins of Asia, reflects a Tethyan origin. The Miocene Anatina burdigalensis from southern France resembles E. spengleri in shell form and we consider it as a species of Exolaternula, the last survivor in western Tethys before the early Miocene closure of the Tethyan Seaway (Harzhauser et al., 2007). Fossils resembling the living Exolaternula liautaudi were present in Japan at least by the mid-Miocene (Itoigawa et al., 1981, 1982). In the Laternula clade the sister position of Laternula elliptica relative to all other species suggests a separation before the diversification of the temperate and tropical species. This is consistent with the scenario that L. elliptica or its precursor was left isolated around Antarctica after the separation and northward movement of Australia with the opening of the Tasman Gateway and onset of the Antarctic Circumpolar Current c. 30 Mya in the early Oligocene (Scher et al., 2015). This final breakup of the Gondwanan–Weddellian Province (Zinsmeister, 1979) would have disrupted larval interchange as Australia progressively moved northwards. Subsequently, as Australia moved into lower latitudes, warmer water species such as L. anatina may have spread into south-east Asia and the northern Indian Ocean while Australia retained a diversity of temperate water endemic species such as L. gracilis, L. creccina and L. tasmanica, or their precursors. The scenario that L. elliptica originated from a southward migration as a more derived taxon (OTT hypothesis; Jablonski et al., 2006, 2013) during a period of polar amelioration can be rejected. A single record from the Pliocene of New Zealand of a fragmentary fossil, Laternula syntheticaMarwick, 1948, with an estimated shell length of 120 mm (later renamed L. laternaLamarck, 1818 by Beu, 2004) was interpreted to have arrived during a warm period. However, the long pallial sinus of this fossil precludes identification as L. laterna (a tropical species), which has a short sinus, and it most closely resembles the south-eastern Australian species, L. gracilis and L. tasmanica. Although it would be desirable to include more samples in the analysis, our results are consistent with an Australian origin for the tropical Laternula. For example, Laternula creccina from temperate southern Australia is a sister species to tropical L. anatina from Papua New Guinea and sub-tropical L. japonica from Japan. Similarly, L. cf. boschasina from Darwin, northern Australia, is a sister species to two tropical species from Singapore and Thailand. Moreover, the diversity of Laternula species around Australia and their wide latitudinal spread compared with other Indo-West Pacific areas is also evidence supporting this idea. Of the Laternula species, L. anatina (Fig. 1E) has the broadest distribution, recorded from Kenya, the Red Sea, the northern Indian Ocean, through south-eastern Asia, northern Australia to Philippines, China and southern Japan. It is also present as a Lessepsian invader into the eastern Mediterranean (Gofas & Zenetos, 2003). Nonetheless, our preliminary molecular results suggest that cryptic species may exist; for example, the frequently synonymized L. japonica is genetically distinct from L. anatina. Other species at lower latitudes have narrower ranges, L. navicula in the northern Indian Ocean, L. boschasina in south-east Asia and L. laterna around northern Australia. Our phylogenetic evidence supports the idea that Laternula elliptica or its precursor was isolated around Antarctica following the split and northward movement of the Australian continent with the opening of the Tasman Gateway and initiation of the Circum-Antarctic Current. Following separation and onset of cooling conditions the species became adapted physiologically to lower temperatures (Peck et al., 2009). Laternula elliptica differs morphologically from congeners in its much larger size, very wide posterior gape, thicker shell (Watson et al., 2012) and prominent periostracum. It also lacks the exterior shell spikes characteristic of all other Laternula species and many other anomalodesmatans (Checa & Harper, 2010). Laternula elliptica is abundant in shallow water around Antarctica particularly at depths of 10–30 m and even intertidally (Waller et al., 2017), with population densities reported up to 65/m2 (Dell, 1990; Zamorano, Duarte & Moreno, 1986). The general lack of durophagous predators (decapod crustaceans and fish) in Antarctic seas (Clarke et al., 2004) could be a contributory factor in its success. By comparison, the lower latitude species of Laternula tend to occupy peripheral marine habitats where predation pressure is probably reduced, such as mangrove fringes (Morton, 1973; Prezant et al., 2008), estuaries with fluctuating salinities (Kang et al., 2006; Kanaya et al., 2008), or locations with elevated salinities such as Shark Bay, Western Australia (Logan & Cebulski, 1970) or the Arabian Gulf (Sheppard et al., 2010). Corroboration of the biogeographical scenarios with a fossil record would be desirable but as already noted the fossil record of Laternula is poor. The only Southern Hemisphere Early Cenozoic occurrence, Laternula sp. from the Eocene Rio Turbio Formation, Santa Cruz Province, Argentina, is part of a still imperfectly known molluscan fauna that does show at least some resemblance to that known from the La Meseta Formation of Seymour Island, north-eastern Antarctic Peninsula (Griffin, 1991). Palaeogeographical reconstructions for the Eocene connection between Tierra del Fuego and the northern tip of the Antarctic Peninsula are complex, but some of the most recent ones, based on new marine geophysical data, place the Rio Turbio basin at a significantly higher palaeolatitude than its present-day position of 51°30′S (Maldonado et al., 2014: fig. 8). It would certainly have been well within Zinsmeister’s (1979, 1982, 1984) Weddellian Province, and Laternula sp. may represent part of the ancestral lineage of L. elliptica. The Rio Turbio Formation does appear to contain a series of distinct sedimentary facies that are missing in the La Meseta Formation, and the two units almost certainly represent slightly different types of shallow marine environment (Griffin, 1991). As a result of recent taxonomic and stratigraphic studies it has been determined that approximately one-third of the 147 gastropod and bivalve species known from the Middle Eocene section of the La Meseta Formation can now be assigned to modern genera (Beu, 2009; Crame et al., 2014). This means that, for at least one key part of the modern Antarctic marine fauna, it was beginning to take shape some 10–15 Mya before the onset of significant global cooling at the Eocene–Oligocene boundary (Zachos, Dickens & Zeebe, 2008). Molecular phylogenetic evidence suggests that the amphipod genus Epimeria, which today forms a species flock in the Southern Ocean, diversified initially in the Middle or Late Eocene (Verheye, Backeljau & d’Udekem d’Acoz, 2017), and the split between the Antarctic/subantarctic limpet Nacella and its temperate to tropical sister taxon Cellana occurred at 32 Mya (González-Wevar et al., 2017). There is even a combination of molecular phylogenetic and biogeographical evidence from the Antarctic terrestrial realm to suggest that a range of taxa had similar Early Cenozoic roots, and have survived to the present day using various types of refugia (Convey et al., 2008). All of this evidence suggests that the Antarctic biota is of considerable ancestry and has been able to adapt to progressive global cooling over a period of tens of millions of years. Laternula had Eocene or even earlier roots in the Antarctic region and was then able to adapt to both the cooling of Antarctica and the warming of the Australian continent as it moved progressively northwards. Despite the present-day diversity and abundance of Laternula species around Australia, the fossil record from there is lacking, with no mention of the genus in Darragh’s (1985) analysis of the Cenozoic molluscan faunas of south-eastern Australia. However, the stratigraphic record is very patchy and suitable facies are not preserved. Coupled with the preferred marginal marine habitats and fragile shells, this may account for the lack of Laternula fossils. However, Pufahl et al. (2004) report Laternula sp. from Pliocene estuarine deposits in the Murray Basin, South Australia. The fossils are preserved as casts and moulds with aragonitic shells dissolved away and identifications were made in the field (N. James, personal communication). If confirmed, these are the only Laternula fossils recorded from Australia. In summary, our molecular results revealed two distinct groups of living Laternulidae. One comprises Exolaternula species possessing a lithodesma and a distribution largely around the northern Indian Ocean and the southern margin of the Asian continent. The Exolaternula clade probably had a Tethyan origin with connections to the western Tethys in the early Miocene but later severed by the closure of the Tethyan Seaway. The more numerous Laternula species lack a lithodesma in the adult, with the Antarctic L. elliptica as a sister taxon to all other species from Australia and central Indo-West Pacific. The Laternula clade probably originated on the Late Gondwanan southern Australia/Antarctica continent, leaving L. elliptica isolated around Antarctica after Australia split and drifted northwards with opening of the Southern Ocean. Temperate and tropical species exist around Australia but we suggest that the tropical species spread and diversified into coastal Asia from the mid-Miocene onwards after the closer approach of Australia. ACKNOWLEGEMENTS For generously providing samples we are grateful to Ruytoro Goto (University of Kyoto), Barbara Buge (MNHN), Konstatin Lutaenko (Russian Academy of Sciences, Vladivostok), Koh Siang Tan (National University of Singapore), Piotr Kuklinski (Institute of Oceanology, Polish Academy of Sciences) and Simon Morley (BAS). Dawn Woods, George Mulvaney and Michael Mulvaney helped collect samples at Burrill Lake, New South Wales. Grateful thanks are due to Tom Schiotte (NHMD) for images of the Mya anserifera holotype, Emmanuel Tardy (MHNG) for images of the lectotype of Anatina laterna, Virginie Héros (MNHN) for arranging opening of valves and images of the holotype of Laternula liautaudi, Konstantin Lutaenko and Elena Chaban (Zoological Museum, St Petersburg) for searching for the type of L. japonica, and Lisa Kirkendale (WAM) and Richard Willan (MAGNT) for images of shells in their collections. David Cothran generously allowed reproduction of his images of living L. elliptica. Tom Darragh (Museum Victoria) advised on Australian fossil faunas, Pierre Lozouet (MNHN) confirmed dating of fossils and Takuma Haga (NMNS, Tokyo) provided information and literature concerning Japanese living and fossil species. We thank Lisa Smith (NHMUK) for help with molecular analyses and Adrian Glover (NHMUK) who facilitated the process. JAC acknowledges financial support from NERC, including NE/I00582X/1. 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APPENDIX Critical assessment of the living species of Laternulidae and their synonyms. Type localities are given where known. Note that the number of considered valid species and nomenclature differs from Huber (2010) and WoRMS. This classification will evolve as more samples are included in molecular analyses. Laternulidae Genus ExolaternulaHabe, 1977 type species: Anatina truncataLamarck, 1818 = L. spengleri (Gmelin, 1792) = L. rostrata (Sowerby, 1839). Lithodesma present. Exolaternula spengleri(Gmelin, 1792) Solen spengleriGmelin, 1792: 3228. Synonyms: Mya anseriferaSpengler, 1793: table 2, fig. 8, holotype NHMD 116367 (Gmelin’s name is based on this specimen and figure), Nicobar Islands; Anatina truncata auct. non Lamarck 1818; Anatina rostrata (G.B. Sowerby II 1839); Anatina limicolaReeve, 1863, Japan; Anatina elegansPhilippi, 1844, China; Anatina berniculaLamy, 1934, Tongatabu. Remarks: Reeve, (1860) used the name A. anserifera for a figured specimen from Tasmania now considered to be Laternula tasmanica, leading to citations of the former in southern Australia (e.g. Morton, 1976). Distribution: Sri Lanka, Southeast Asia, northern Australia, Philippines, China, southern Japan (Ryukyu Islands). Exolaternula liautaudi (Mittre, 1844) Anatina liautaudiMittre, 1844:16, pl. 104, holotype MNHN-IM- 2000-33234. Manila, Philippines. Image: https://science.mnhn.fr/institution/mnhn/collection/im/item/2000-33234 Synonyms: Laternula limicola auct. non Reeve, 1863; L. navicula auct. non Reeve, 1863; L. marilina auct. non Reeve, 1860; L. gracilis auct. non Reeve, 1860; Anatina kamakuranaPilsbry, 1895, Kamakura, Japan; Anatina pechiliensisGrabau & King, 1928, Peitaiho, NW China; Laternula nanhaiensisZhuang & Cai, 1982, Hepu, Guangxi. Remarks: There has been much nomenclatural confusion concerning this species; in Japanese, Chinese and Russian literature it is often cited as L. marilina, an Australian species lacking a lithodesma and now synonymized with L. gracilis. Comparison of type specimens shows that L. liautaudi, originally described from the Philippines, is the earliest name. Distribution: Northern Philippines, China, Taiwan, Korea, Japan and eastern Russia (Peter the Great Bay), exotic to north-west America. Exolaternula erythraea (Morris & Morris, 1993) Laternula (Exolaternula) erythraeaMorris & Morris, 1993: 8, 19, holotype NHMUK 1992175, Fujairah, United Arab Emirates. Remarks: L. erythraensis was used in error for L. erythraea (e.g. Oliver, 1995; Feulner & Hornby, 2006). Distribution: Arabian Gulf, Gulf of Oman. Genus LaternulaRöding, 1798, type species: Solen anatinusLinnaeus, 1758. Synonym: LaternulinaHabe 1952, type species Anatina japonicaLischke, 1872. Lithodesma absent in adult. Laternula anatina (Linnaeus, 1758) Solen anatinusLinnaeus 1758: 673. Synonyms: Anatina subrostrataLamarck, 1818; Anatina hispidulaCuvier, 1829; Anatina amphoraReeve, 1863, Island of Burias, Philippines; Anatina cumingiReeve, 1863, Amboina; Anatina eximiaReeve, 1863; Anatina flexuosaReeve, 1863, Japan; Anatina labiataReeve, 1863, Ceylon; Anatina siphonataReeve, 1863, Borneo. Remarks: No type material for S. anatinus exists. Linnaeus based the name on the figure in Rumphius (1705: pl. 45 f O and subsequent editions) with locality given as ‘O. Asiatici’. The figure is poor but has the upturned posterior ‘beak’ of shells identified as this species. It is also figured in Chemnitz (1782: 62, pl. 6, figs 46–48) and according to Lamy (1934),Lamarck (1818) based his name A. subrostrata on these figures. Distribution: East Africa (rare), Red Sea, SE Asia, NW Australia, Philippines, China, Okinawa, southern Japan. Exotic to eastern Mediterranean. Laternula elliptica (King, 1832) Anatina ellipticaKing, 1832: 335, holotype NHMUK 197528, South Shetland Islands. Synonym: Anatina prismaticaSowerby, 1834, South Shetland Islands. Remarks: Usually cited as described by Broderip & King (1832) but see Coan, Petit & Zelaya (2011) for authorship. Distribution: Circum-Antarctica, Kerguelen, South Georgia, South Shetland Islands. Laternula boschasina (Reeve, 1860) Anatina boschasinaReeve, 1860, pl. 2, fig. 13, syntypes NHMUK 197513/1–3, Negros Island, Philippines. Remarks: Our sequenced species from Darwin is much smaller than the syntypes but has a similar deep sinus, commarginal folds and brown periostracal margin. Distribution: Uncertain but includes south-east Asia and northern Australia. Laternula bullata (Reeve, 1863) Anatina bullataReeve, 1863, pl. 1 fig. 3, syntypes NHMUK 197513/1–3, Sibonga, Zebu, Philippines. Remarks: The species sequenced from Singapore (sometimes called L. boschasina) is similar to the type with a rounded anterior, tapering posterior and shallow pallial sinus. Distribution: Southeast Asia. Laternula corrugata (Reeve, 1863) Anatina corrugataReeve, 1863, pl. 4, fig. 25, NHMUK 197523/1–2, Ticao Island, Philippines. Remarks: The species sequenced from Shark Bay, Western Australia, is broadly similar to syntypes of this species but may be distinct. Distribution: Philippines, ?Western Australia. Laternula creccina (Reeve, 1860) Anatina creccinaReeve, 1860, pl. 2 fig. 12, NHMUK 197512/1–2, Adelaide, Australia. Synonyms: Anatina vaginaReeve, 1863, Moreton Bay, Australia; Anatina attenuataReeve, 1863, Sydney, Australia. Remarks: The Moreton Bay locality for A. vagina is probably erroneous. Distribution: South-eastern, southern and south-western Australia. Laternula gracilis (Reeve, 1860) Anatina gracilisReeve, 1860, pl. 2 fig. 9, NHMUK 19759/1–3, Moreton Bay, Queensland. Synonyms: Anatina marilinaReeve, 1860, Australia; Anatina rectaReeve, 1863, Port Phillip, Victoria, Australia; ?Anatina tasmanicaReeve, 1863, Tasmania. Remarks: Molecular analysis indicates that specimens identified as three species above are monospecific with L. gracilis taking priority. The status of the largest species, L. tasmanica, is uncertain but shares characters with L. gracilis. Distribution: Eastern Australia from southern Queensland to Victoria and Tasmania. Laternula impura (Pilsbry 1901) Anatina impuraPilsbry, 1901: 208, pl. 19 fig. 9, syntypes ANSP 68536, Sagami, Japan. Remarks: The status of this species is uncertain. Distribution: Southern Japan Laternula japonicaLischke, 1872: 107; fig. 1874, pl. 9, figs 7–10, types not located, Tokyo, Japan. Remarks: This species is often synonymized with L. anatina but our molecular results indicate it is genetically distinct. An earlier name may be Anatina blainvilleiReeve, 1863, pl. 3, fig 17, Island of Burias, Philippines. Distribution: Southern Japan. Laternula laterna (Lamarck, 1818) Anatina laternaLamarck 1818: 463, lectotype MNHG 1082/33 selected Beu (2004: 184, fig. 18C–E). Synonyms: Anatina cistellaReeve, 1863, Moluccas; Anatina constricta, Reeve, 1863, northern Australia; A. valenciennesiiReeve, 1863, China. Remarks: The lectotype is a large specimen with a short posterior beak and differs from the Lamarckian syntype specimens (now paralectotypes) labelled A. laterna in MNHN Paris (Lamy, 1934, pl. 1, fig. 7). Distribution: Northern Australia, Indonesia. Beu (2004) wrongly states, citing Lamprell & Healy (1998: 214), that the distribution ranges from southern Western Australia to South Australia, Victoria, Tasmania and New South Wales. Laternula navicula (Reeve, 1863) Anatina naviculaReeve, 1863, pl. 4 fig. 21, NHMUK 197520/1–3, type locality not cited. Synonyms: Anatina barkudaensis Preston, 1915, Lake Chilka, India; Anatina barkulensisPreston, 1915, Lake Chilka; Anatina granulosaPreston, 1914, Lake Chilka; Anatina smithiPreston, 1905, Sri Lanka. Distribution: NW Indian Ocean, Arabian Sea, India, Sri Lanka, Andaman Sea. Laternula sp. Remarks: This species, collected in Kungkraben Bay, Thailand, and called L. corrugata by Prezant et al. (2008) and then changed to L. anatinaPrezant et al. (2015), is neither of these taxa. It is broadly similar in shape to L. bullataReeve, 1860 but molecularly distinct from Singapore specimens that we identify as that species. The following species are of uncertain status; all are small shells and probably juveniles. Anatina fabaReeve, 1863, pl. 4, fig. 22, Brisbane, type not located. Anatina argenteaReeve, 1863, pl. 4, fig. 29, NHMUK 197526. Anatina prolongataReeve, 1863, pl. 4, fig. 28, Port Curtis, Queensland, type not located. © 2018 The Linnean Society of London, Biological Journal of the Linnean Society http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Biological Journal of the Linnean Society Oxford University Press

Left in the cold? Evolutionary origin of Laternula elliptica, a keystone bivalve species of Antarctic benthos

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Abstract

Abstract The large, burrowing bivalve Laternula elliptica is an abundant component of shallow-water soft-substrate communities around Antarctica but its congeners are temperate and tropical in distribution and their phylogenetic relationships are obscure. A new molecular analysis of Laternulidae species shows that there are two distinct clades, one of Exolaternula species, E. spengleri and E. liautaudi, possessing a ligamental lithodesma and a larger clade of species lacking the lithodesma. Of the latter, Laternula elliptica is a sister taxon to temperate and tropical species, including those that live around the coasts of Australia from Tasmania to Darwin. It is suggested that L. elliptica was left isolated around Antarctica following the opening of the Tasman Gateway and initiation of the Circum-Antarctic Current as Australia drifted northwards following the final breakup of Gondwana. A further scenario is that as Australia moved closer to Asia, species spread into tropical habitats and more widely to the Red Sea and Japan. Exolaternula species have a likely Tethyan origin and the present-day range is from the Arabian Gulf, around southern Asia and as far north as southern Russia. INTRODUCTION Although the precise origins of the modern Antarctic marine fauna are undoubtedly complex, there has always been a distinct impression that certain elements within it are both of considerable antiquity and endemic to the southern high latitudes (Lipps & Hickman, 1982; Clarke & Crame, 1989). In all probability these taxa date back to at least the Late Cretaceous – Early Palaeogene, a time when the southern margins of the Gondwana supercontinent were still more or less intact, and polar climates were significantly warmer than those of today. Zinsmeister’s (1982) extensive shallow marine Weddellian Province, stretching from southern Patagonia through western Antarctica to New Zealand and eastern Australia, was established on the basis of various endemic molluscan families, one of which, the Struthiolariidae (Littorinimorpha; Stromboidea), still occurs in the region (Beu, 2009). As our knowledge of both the fossil record and the molecular phylogenetics of Antarctic marine taxa has steadily improved, it is becoming appropriate to ask how certain specific elements within the fauna may have evolved. Do their roots lie in some form of ancestral Weddellian province, or were they more recent immigrants? This sort of question is particularly apposite for the very common infaunal bivalve Laternula elliptica (Anomalodesmata; Laternulidae), as its congeners can be traced northwards through temperate South Australia into the heart of the tropical Indo-Pacific realm, and then northwards again into the temperate North-West Pacific. Is this a genus that spread either into or out of Antarctica, and if so, when? Laternula elliptica (King, 1832) is a large (> 100 mm) infaunal bivalve abundant in shallow water and even intertidal habitats around the Antarctic continent and sub-Antarctic islands (Fig. 1A–C). Its abundance and prominence in benthic communities, and its rank as a keystone species by Harper et al. (2012), has attracted considerable research interest with a multitude of publications investigating many aspects of its biology and ecology. A few examples include: physiology (Morley et al., 2009, 2012), biochemistry (González & Puntarulo, 2011), reproduction (Kang, Ahn & Choi, 2003), growth rates (Ralph & Maxwell, 1977; Brey et al., 2011), burrowing behaviour (Peck et al., 2009), trace metals (Ahn et al., 1996), shell microstructure and mineralogy (Sato-Okoshi & Okoshi, 2008; Nehrke et al., 2012), ice scour damage (Harper et al., 2012) and proteomics (Clark et al., 2010). Figure 1. View largeDownload slide Laternula elliptica, type species of Exolaternula and Laternula, and fossil Laternulidae. A. Laternula elliptica (King, 1832), James Ross Island, Antarctica (NHMUK), L = 69 mm. B, C. Laternula elliptica, in life position with fused inhalant and exhalant siphons. Images by David Cothran/Lindblad Expeditions, All Rights Reserved. D. Exolaternula spengleri (Gmelin, 1792) (senior synonym of A. truncata, A. rostrata), Port Essington, Australia (NHMUK), L = 78.4 mm. E. Laternula anatina (Linnaeus, 1758), Moluccas (NHMUK), L = 55.2 mm. F. Laternula elliptica, Early Pliocene, Cockburn Island Formation, Cockburn Island, north-eastern Antarctic Peninsula (BAS DJ. 351.21), L = 138 mm. G. Laternula burdigalensis (Cossmann & Peyrot, 1909), Miocene, Salles, France, L = 80 mm (from Cossmann & Peyrot, 1909). H, I. Laternula. sp., Eocene, Rio Turbio Formation, Patagonia, Argentina, L = 50 mm, from Griffin (1991) with permission Journal of Paleontology. Figure 1. View largeDownload slide Laternula elliptica, type species of Exolaternula and Laternula, and fossil Laternulidae. A. Laternula elliptica (King, 1832), James Ross Island, Antarctica (NHMUK), L = 69 mm. B, C. Laternula elliptica, in life position with fused inhalant and exhalant siphons. Images by David Cothran/Lindblad Expeditions, All Rights Reserved. D. Exolaternula spengleri (Gmelin, 1792) (senior synonym of A. truncata, A. rostrata), Port Essington, Australia (NHMUK), L = 78.4 mm. E. Laternula anatina (Linnaeus, 1758), Moluccas (NHMUK), L = 55.2 mm. F. Laternula elliptica, Early Pliocene, Cockburn Island Formation, Cockburn Island, north-eastern Antarctic Peninsula (BAS DJ. 351.21), L = 138 mm. G. Laternula burdigalensis (Cossmann & Peyrot, 1909), Miocene, Salles, France, L = 80 mm (from Cossmann & Peyrot, 1909). H, I. Laternula. sp., Eocene, Rio Turbio Formation, Patagonia, Argentina, L = 50 mm, from Griffin (1991) with permission Journal of Paleontology. Outside of the Southern Ocean, Laternula species range from the southern temperate zone (Tasmania) through subtropical and tropical Australia, south-eastern Asia, Philippines, China and Japan as far north as Peter the Great Bay in western Russia; and to the west through the northern Indian Ocean, Arabian Gulf, Red Sea and, rarely, to East Africa, but they are absent from oceanic islands. One species, L. liautaudi, is exotic to west coast USA (Miller, Coan & Chapman, 1999 as L. marilina; or L. gracilisFofonoff et al., 2017) and another, L. anatina, to the eastern Mediterranean (Gofas & Zenetos, 2003). The genus is particularly speciose around Australia from where 12 nominal species have been described or recorded. By contrast to the research focus on L. elliptica, there are relatively few studies devoted to the temperate and tropical species of Laternula and most aspects of their biology and systematics remain uninvestigated. Exceptions are the morphological and ecological studies of Laternula rostrata by Morton (1973, 1976), Adal & Morton (1973) and Prezant et al. (2008), the physiology of species from Singapore and South Australia (Morley et al., 2009; Lai et al., 2011) and China (Zhuang, 2005), and ecological studies on Korean and Japanese species (Kang et al., 2006; Kanaya, Takagi & Kikuchi, 2008). Laternula species have thin, elongate, nacreous and granular prismatic shells, a posterior gape and an external surface covered in short spikes (Checa & Harper, 2010). There is a prominent umbonal slit in the shell with an internal shell buttress posterior to the hinge (Savazzi, 1990). The internal ligament is set on a chondrophore, and an anterior, transverse lithodesma (a calcified ossicle within the ligament) is present in some species. Siphons are long, fused and periostracum-covered (Fig. 1), with distal tentacles and siphonal eyes (Morton, 1973; Adal & Morton, 1973). The ventral mantle is fused, with a small pedal gape, and the foot is small. Arenophilic mantle glands are present on siphons (Sartori, Passos & Domaneschi, 2006) and their sand adherent secretions are present on juvenile shells < 10 mm long (E. M. Harper, unpub. obs). Laternulids live in muddy, intertidal or shallow subtidal habitats, often amongst or near mangroves (Prezant et al., 2008; Lai et al., 2011), in seagrass beds (our personal observations) and frequently in habitats of fluctuating or elevated salinities. Compared with its lower latitude congeners, Laternula elliptica is larger, thicker shelled (Watson et al., 2012; Prezant, Shell & Wu, 2015) and lacks the spikes (spinules) on the shell surface present in all other species. Apart from L. elliptica, discrimination of Laternula species is extremely confused and misidentifications abound. There is no real agreement on the number of living species; the latest taxonomic account (Huber, 2010) recognized 19 species (20 species in WoRMS, 2017), while previously Lamy (1934) documented 15–20 species and in the best illustrated of the 19th century monographs Reeve (1860–1863) illustrated 30 species with 24 of these described as new. The type specimens from Reeve (NHMUK) are a major resource for any taxonomic study of the genus. We agree with Huber (2010) that species depictions and distributional data in many identification guides (e.g. Lamprell & Healy, 1998) and other publications (Morton, 1976) are wrongly assigned and have led to continuing confusion. Laternula species have been divided into two subgenera (Habe, 1977) on the basis of the presence (Exolaternula) or absence (Laternula) of a lithodesma. Nevertheless, the taxonomic or phylogenetic significance of this character has been doubted (Huber, 2010). In a broader context, molecular analyses (Harper, Dreyer & Steiner, 2006; Combosch et al., 2017; Williams et al., 2017) place Laternula within the Anomalodesmata in a clade with Lyonsiidae, Clavagellidae and Pandoridae but distinct from Cochlodesma (Periplomatidae) which has a similar umbonal slit but which groups with Thraciidae and Myochamidae. Clearly, L. elliptica is a prominent and ecologically important element in Antarctic benthic faunas but is biogeographically isolated from the warmer water species of the genus. In this study we use a molecular analysis to investigate the phylogenetic relationships of L. elliptica to the lower latitude species and evaluate three possible biogeographical scenarios concerning its present isolation in polar seas. Is L. elliptica a relict species dating from a former, broader, distributional range of the genus and warmer Antarctic conditions (e.g. during the Early–Middle Eocene) but now isolated by the formation of the Circum-Antarctic Current and has subsequently become physiologically adapted to cold conditions? An expectation arising from this scenario might be that L. elliptica is most closely related to the temperate southern Australian species. Another possibility is that Laternula species originated on Late Gondwanan shallow shores and rafted northwards with Australia into the tropics after the split from Antarctica c. 30 Mya, leaving L. elliptica isolated in the Southern Ocean. This may account for the diversity of Laternula species around Australia from temperate conditions around Victoria/Tasmania to tropical waters to the north. Laternula species then spread and diversified into tropical Asian shallow-water environments. An expectation would be that L. elliptica is sister to all other species or groups with the Australian taxa. A further scenario that matches the ‘out of the tropics’ (OTT) model developed by Jablonski, Roy & Valentine (2006) and Jablonski et al. (2013) is that Laternula diversified on tropical–subtropical shores and later spread southwards into Antarctica during warmer periods, with L. elliptica as a derived species. MATERIAL AND METHODS Molecular methods The DNA extraction and amplification protocols of Williams et al. (2013) were used to amplify portions of four genes from 16 specimens (Table 1). The genes amplified were the nuclear 28S rRNA gene (approximately 1640 bp) and three mitochondrial genes: 12S rRNA gene (approximately 610 bp), 16S rRNA gene (approximately 500 bp) and cytochrome b (405 bp). Lyonsia norwegica (Lyonsiidae) and Bryopa lata (Clavagellidae) were used as outgroups having been shown in previous analyses to be sister groups of Laternulidae (Harper et al., 2006; Combosch et al., 2017; Williams et al., 2017). Sequence reactions were performed directly on purified PCR products using the BigDye Terminator v1.1 Cycle Sequencing Kit (Applied Biosystems) and run on an Applied Biosystems 3730 DNA Analyzer automated capillary sequencer. Sequences for each gene fragment were assembled and edited using Sequencher (v.5.1; Gene Codes Corporation). Table 1. Laternulidae species included in the analysis with collection localities, locality codes used in Figure 2, museum registration numbers for vouchers and GenBank accession numbers for the genes sequenced for each taxon   Collection locality  Locality code  Voucher number  28S  cyt B  12S  16S  Exolaternula liautaudi (Mittre, 1844)  Olga Bay, Eastern Russia, 43°41′56″N, 135°15′04″E  OB 1  NHMUK 20170326  LT960470  LT960693  LT960373  LT960384  Exolaternula liautaudi (Mittre, 1844)  Olga Bay, Eastern Russia, 43°41′56″N, 135°15′04″E  OB 2  NHMUK 20170327  LT960471  LT960694  LT960374  LT960385  Exolaternula liautaudi (Mittre, 1844)  Kojima-Shinden, Kawasaki, Japan, 35°30′52″N, 139°48′29″E  KS  NHMUK 20170328  LT960472  LT960695    LT960386  Exolaternula spengleri (Gmelin, 1792)  Casiguran Bay, Luzon, Philippines, 16°15.95′N, 122°05′E  LP  MNHN IM-2007-41446  LT960473      LT960387  Exolaternula spengleri (Gmelin, 1792)  Sungei Buroh, Singapore, 1°26′39″N, 103°43′39″E  SIN  NHMUK 20160581  LT960474  KX815963  KX815963  KX815967  Laternula elliptica (King, 1832)  Rothera Point, Adelaide Island, Antarctica, 67°34′S, 68°08′W  RO  no voucher  LT960475  KX815959  KX815959  KX815959  Laternula elliptica (King, 1832)  King George Island, South Shetland Islands, 62°09.87′S, 58°33.83′W  SS  NHMUK 20170329  LT960476  LT960696    LT960388  Laternula creccina (Reeve, 1860)  Esperance, Bandy Creek, W. Australia, 33°49′50″S, 121°56′10″E  ESP  NHMUK 20030177  LT960477  LT960697    LT960389  Laternula anatina (Linnaeus, 1758)  Papua New Guinea, near Rempi, stn PR104, 5°5′6″ S,145°48′E  PNG  MNHN IM-2013-15152  LT960478  LT960698  LT960375  LT960390  Laternula japonica (Lischke, 1872)  Hakata-jima Island, Ehime pref., Japan, 34°12′N, 133°05′E  HJ  NHMUK 20170330  LT960479    LT960376  LT960391  Laternula cf. boschasina (Reeve, 1860)  Ludmilla Creek, Darwin, Australia, 12°24′28″S, 130°50′07″E  DAR  NHMUK 20170331  LT960480  LT960699  LT960377    Laternula cf. bullata (Reeve, 1860)  Sungei Buroh, Singapore; 1°26′39″′N, 103°43′39″E  SIN  NHMUK 20170332  LT960481  LT960700  LT960378  LT960392  Laternula sp.  Kungkraben Bay, Thailand, 12°34.42′N, 101°54.24′E  KK  NHMUK 20170333  LT960482  LT960701  LT960379  LT960393  Laternula cf. corrugata (Reeve, 1863)  Denham, Shark Bay, W. Australia, 25°54′11″S, 118°31′16″E  SB  NHMUK 20170334  LT960483  LT960702  LT960380  LT960394  Laternula gracilis (Reeve, 1860)  Geelong, Victoria, Australia, 38°9′07″S, 144°23′44″E  GE 1  NHMUK 20170335    LT960703  LT960381  LT960395  Laternula gracilis (Reeve, 1860)  Geelong, Victoria, Australia, 38°9′07″S, 144°23′44″E  GE 2  NHMUK 20170336  LT960484    LT960382  LT960396  Laternula gracilis (Reeve, 1860)  Burrill Lake, NSW, Australia, 35°22′03″S, 150°26′04″E  BL  NHMUK 20170337  LT960485  LT960704  LT960383  LT960397  Laternula gracilis (as L. marilina in Taylor et al., 2007)  N. Stradbroke Island, Moreton Bay, Qld, Australia, 27°24′29″S, 153°24′42″E  MB 1  NHMUK 29970221  AM779661        Laternula gracilis (Reeve, 1860)  N. Stradbroke Island, Moreton Bay, Queensland, Australia  MB 2  Combosch et al., (2017)  KX713395      KX713227  Outgroups  Bryopa lata (Broderip, 1834)  Singapore, 1°13.9′N, 103°52′E    NHMUK 20160581  LT960486  KX815957  KX815957  KX815957  Lyonsia norwegica (Gmelin, 1792)  Tjärno, Sweden, 58°52.42′N, 11°06.18′E    NHMUK 20160584  LT960487  KX815960  KX815960  KX815960    Collection locality  Locality code  Voucher number  28S  cyt B  12S  16S  Exolaternula liautaudi (Mittre, 1844)  Olga Bay, Eastern Russia, 43°41′56″N, 135°15′04″E  OB 1  NHMUK 20170326  LT960470  LT960693  LT960373  LT960384  Exolaternula liautaudi (Mittre, 1844)  Olga Bay, Eastern Russia, 43°41′56″N, 135°15′04″E  OB 2  NHMUK 20170327  LT960471  LT960694  LT960374  LT960385  Exolaternula liautaudi (Mittre, 1844)  Kojima-Shinden, Kawasaki, Japan, 35°30′52″N, 139°48′29″E  KS  NHMUK 20170328  LT960472  LT960695    LT960386  Exolaternula spengleri (Gmelin, 1792)  Casiguran Bay, Luzon, Philippines, 16°15.95′N, 122°05′E  LP  MNHN IM-2007-41446  LT960473      LT960387  Exolaternula spengleri (Gmelin, 1792)  Sungei Buroh, Singapore, 1°26′39″N, 103°43′39″E  SIN  NHMUK 20160581  LT960474  KX815963  KX815963  KX815967  Laternula elliptica (King, 1832)  Rothera Point, Adelaide Island, Antarctica, 67°34′S, 68°08′W  RO  no voucher  LT960475  KX815959  KX815959  KX815959  Laternula elliptica (King, 1832)  King George Island, South Shetland Islands, 62°09.87′S, 58°33.83′W  SS  NHMUK 20170329  LT960476  LT960696    LT960388  Laternula creccina (Reeve, 1860)  Esperance, Bandy Creek, W. Australia, 33°49′50″S, 121°56′10″E  ESP  NHMUK 20030177  LT960477  LT960697    LT960389  Laternula anatina (Linnaeus, 1758)  Papua New Guinea, near Rempi, stn PR104, 5°5′6″ S,145°48′E  PNG  MNHN IM-2013-15152  LT960478  LT960698  LT960375  LT960390  Laternula japonica (Lischke, 1872)  Hakata-jima Island, Ehime pref., Japan, 34°12′N, 133°05′E  HJ  NHMUK 20170330  LT960479    LT960376  LT960391  Laternula cf. boschasina (Reeve, 1860)  Ludmilla Creek, Darwin, Australia, 12°24′28″S, 130°50′07″E  DAR  NHMUK 20170331  LT960480  LT960699  LT960377    Laternula cf. bullata (Reeve, 1860)  Sungei Buroh, Singapore; 1°26′39″′N, 103°43′39″E  SIN  NHMUK 20170332  LT960481  LT960700  LT960378  LT960392  Laternula sp.  Kungkraben Bay, Thailand, 12°34.42′N, 101°54.24′E  KK  NHMUK 20170333  LT960482  LT960701  LT960379  LT960393  Laternula cf. corrugata (Reeve, 1863)  Denham, Shark Bay, W. Australia, 25°54′11″S, 118°31′16″E  SB  NHMUK 20170334  LT960483  LT960702  LT960380  LT960394  Laternula gracilis (Reeve, 1860)  Geelong, Victoria, Australia, 38°9′07″S, 144°23′44″E  GE 1  NHMUK 20170335    LT960703  LT960381  LT960395  Laternula gracilis (Reeve, 1860)  Geelong, Victoria, Australia, 38°9′07″S, 144°23′44″E  GE 2  NHMUK 20170336  LT960484    LT960382  LT960396  Laternula gracilis (Reeve, 1860)  Burrill Lake, NSW, Australia, 35°22′03″S, 150°26′04″E  BL  NHMUK 20170337  LT960485  LT960704  LT960383  LT960397  Laternula gracilis (as L. marilina in Taylor et al., 2007)  N. Stradbroke Island, Moreton Bay, Qld, Australia, 27°24′29″S, 153°24′42″E  MB 1  NHMUK 29970221  AM779661        Laternula gracilis (Reeve, 1860)  N. Stradbroke Island, Moreton Bay, Queensland, Australia  MB 2  Combosch et al., (2017)  KX713395      KX713227  Outgroups  Bryopa lata (Broderip, 1834)  Singapore, 1°13.9′N, 103°52′E    NHMUK 20160581  LT960486  KX815957  KX815957  KX815957  Lyonsia norwegica (Gmelin, 1792)  Tjärno, Sweden, 58°52.42′N, 11°06.18′E    NHMUK 20160584  LT960487  KX815960  KX815960  KX815960  MNHN, Muséum national dHistoire Naturelle, Paris; NHMUK, The Natural History Museum, London. View Large Figure 2. View largeDownload slide Combined gene tree for Laternulidae based on sequences from four genes (28S rRNA, 12S, 16S and cyt b) using Bayesian inference as implemented by MrBayes. Support values are posterior probabilities (PP). Images are of sequenced specimens or proxies – not to scale. Colour code on localities denotes: tropical (red), temperate (green) and Antarctic (blue) Locality codes used on the tree: BL – Burrill Lake, New South Wales, Australia; DAR – Darwin, Australia; ESP – Esperance, Western Australia; HJ – Higata-Jima Island, Japan; GE – Geelong, Victoria, Australia; KK – Kungkraben Bay, Thailand; KS – Kojima-Shinden, Japan; LP – Luzon, Philippines; MB – Moreton Bay, Queensland, Australia; OB – Olga Bay, eastern Russia; PNG – Papua New Guinea; RO – Rothera, Adelaide Island, Antarctica; SB – Shark Bay, Western Australia; SIN – Singapore; SS – South Shetland Islands. Figure 2. View largeDownload slide Combined gene tree for Laternulidae based on sequences from four genes (28S rRNA, 12S, 16S and cyt b) using Bayesian inference as implemented by MrBayes. Support values are posterior probabilities (PP). Images are of sequenced specimens or proxies – not to scale. Colour code on localities denotes: tropical (red), temperate (green) and Antarctic (blue) Locality codes used on the tree: BL – Burrill Lake, New South Wales, Australia; DAR – Darwin, Australia; ESP – Esperance, Western Australia; HJ – Higata-Jima Island, Japan; GE – Geelong, Victoria, Australia; KK – Kungkraben Bay, Thailand; KS – Kojima-Shinden, Japan; LP – Luzon, Philippines; MB – Moreton Bay, Queensland, Australia; OB – Olga Bay, eastern Russia; PNG – Papua New Guinea; RO – Rothera, Adelaide Island, Antarctica; SB – Shark Bay, Western Australia; SIN – Singapore; SS – South Shetland Islands. Mitochondrial genes of another four taxa, Lyonsia norwegica, Bryopa lata, Laternula elliptica (Antarctica) and Laternula rostrata (Singapore, herein E. spengleri), were previously published as complete, or nearly complete, mitochondrial genomes (Williams et al., 2017) and 12S, 16S and cytB sequence data were taken from these sequences (GenBank accession numbers KX815957, KX815959, KX815960 and KX815963). Sequences for 28S rRNA genes were obtained from the same NGS genomic data set used in Williams et al. (2017) to assemble mitochondrial genomes. Briefly, genomic DNA was sequenced on one-fifth of a flowcell on an Illumina MiSeq platform (v.2 chemistry; 2 × 250 paired-end). Reads were analysed and assembled using Geneious (v.8.1.8; https://www.geneious.com). The data were trimmed allowing no ambiguous base calls and removing bases from the terminal ends of reads with an error probability of 0.05 or higher (i.e. those with a greater than 5% chance of being incorrect). The trimmed reads were first assembled de novo and the resulting contigs were interrogated against the NCBI database, using BLAST (Altschul et al. 1990), in order to identify ribosomal gene sequences. Gene boundaries were determined by comparison with other molluscan taxa. Coverage data are available in Williams et al. (2017). Phylogenetic datasets analysed included three individual gene datasets and a combined gene dataset including all individuals that had sequences for at least three genes. Alignment of cytB sequences was unambiguous and no stop codons were observed. Sequences of ribosomal genes were aligned in Geneious (v.8.1.8) using ClustalW. Poorly aligned sites in the ribosomal gene alignments were identified using the online Gblock server using all three options for a less stringent selection (v.0.91b; Castresana, 2000, http://molevol.cmima.csic.es/castresana/Gblocks_server.html) and removed from alignments. After removal of ambiguously aligned blocks of data, a total of 2922 bp of aligned sequence remained to be used in phylogenetic analyses for the combined gene dataset (90% of the original 3241positions). In individual analyses, alignment lengths after Gblocks were 444 bp of sequence from 16S rRNA (89% of 495 bp in the original alignment), 539 bp of 12S rRNA (90% of 597 bp in the original alignment) and 1575 bp of 28S rRNA (88% of 1785 bp in the original alignment). The best nucleotide substitution models were determined using jModelTest (v.X; Darriba et al. 2012) using the Akaike information criterion (AIC). The best nucleotide substitution models were for cytB HKY+I+G and for all three rRNA genes GTR+I+G. These models were used in Bayesian phylogenies implemented in MrBayes (v.3.2.6; Huelsenbeck & Ronquist, 2001). The analysis ran for 10000000 generations, with a sample frequency of 1000. The first 10% were discarded as burn-in after checking that runs had reached stationarity. Stationarity was determined by examining traces in TRACER (v.1.6 http://tree.bio.ed.ac.uk/software/tracer/). Convergence between the two runs was tested by examining traces using TRACER and by checking that the potential scale reduction factors produced by the ‘sump’ command in MrBayes were close to one (Gelman & Rubin, 1992) and that the mean standard deviation of split frequencies approached zero. Taxonomic rationale Because the species taxonomy of Laternula is so confused, care was taken to identify the taxa included in the molecular analyses. Type material of Laternula species was examined in NHMUK and MNHN along with images of other relevant specimens from ANSP, NHMD, MHNG and WAM. Using these, plus the taxonomic revisions of Reeve (1860), Lamy (1934) and most recently Huber (2010) and figures in regional faunas (e.g. Lamprell & Healy, 1998; Okutani, 2000; Lutaenko & Noseworthy, 2012) augmented by the results of our molecular analysis herein, we have derived an outline taxonomic classification (Appendix) listing what we believe are extant species and their synonyms. Notable taxonomic changes resulting from study of type material (NHMD) are that Solen spengleriGmelin, 1792 (herein Exolaternula spengleriFig. 1D) is an earlier name for the species variously called L. anserifera (Spengler, 1793), L. truncata (Lamarck, 1818 auct.) or L. rostrata (Sowerby, 1839). Images of newly separated valves of the holotype of Anatina liautaudiMittre, 1844 (MNHN IM–2000–33234) indicate that it is the earliest name (herein as Exolaternula liautaudi) for the variously named north-east Asian margin species. Also, genetic data (herein) show that the Australian species variously identified as Laternula gracilis, L. marilina and L. recta are a single species, with L. gracilis (Reeve, 1860) having priority. Our present estimate is that there are 15 living species of Laternulidae; further and more comprehensive sampling will probably resolve some problem areas but may also reveal the existence of cryptic species. Institutional abbreviations: ANSP, Academy of Natural Sciences Philadelphia at Drexel University, USA; BAS, British Antarctic Survey, Cambridge, UK; MAGNT, Museum and Gallery of Northern Territory, Australia; MHNG, Muséum d’histoire naturelle, Geneva, Switzerland; MNHN, Muséum national d’Histoire naturelle, Paris, France; NHMD, Natural History Museum of Denmark, Copenhagen; NHMUK, The Natural History Museum, London, UK; WAM, Western Australian Museum, Perth, WA. RESULTS All individual gene trees had similar topologies to each other and to the combined gene tree shown in Figure 2. A clear result is that the sequenced Laternulidae species split into two major groups, one comprising L. spengleri from Singapore and Philippines and L. liautaudi from Japan and south-eastern Russia and a second, larger group containing all the other species including L. elliptica. A robust topology in all gene trees is that, in the larger clade, Laternula elliptica is the sister group, with maximum support (P = 1.0), to all the other Laternula species from Australia, south-eastern Asia and southern Japan. Amongst the temperate and tropical samples are three well-supported sub-clades. One consists of three Laternula collected from near Esperance (southern Western Australia), Papua New Guinea and southern Japan; these are similar to Laternula anatina in shell form but are genetically different from each other and we have identified them as L. creccina, L. anatina and L. japonica. The cooler water Laternula creccina is the sister group to the two warm water species. A second sub-clade includes three samples collected at Darwin, Singapore and eastern Thailand but differ from each other in the molecular tree. The sample from Darwin is closest in shell characters to L. boschasina. The specimen from Singapore resembles the syntypes of L. bullata and differs from the Kungkraben Bay, Thailand, example which we retain as Laternula sp. The third sub-clade comprises Laternula from southern and eastern Australia [Port Phillip Bay (Victoria), Burrill Lake (New South Wales) and Moreton Bay (Queensland)]. Laternula from these locations have been variously named in collections as L. gracilis, L. recta and L. marilina but these have only minor genetic differences, suggesting that they are conspecific, with L. gracilis having taxonomic priority. A species from Shark Bay, Western Australia, that we identify as L. cf. corrugata, is a sister to the eastern Australian Laternula gracilis. Geological record of Laternula Other anomalodesmatans possessing an umbonal slit (Periplomatidae) have been confused with Laternula, especially in fossils, and many records of fossil Laternula can be discounted. For example, the so-called Laternula fuchsi (Hoernes, 1875) widely reported from the Miocene (Burdigalian) of eastern Europe (Harzhauser, Mandic & Schlögl, 2011) is a periplomatid, as is Laternula ravniSchnetler, 2001 from the Palaeocene of Denmark. Furthermore, the ‘Laternula’ species widely reported from the Cenozoic of far Eastern Russia are now classified as Periplomatidae (Kafanov, Ogasawara & Marincovich, 2001). A search of the fossil literature for records of bivalves that resemble our concept of Laternula indicates that they are rare. This may be a consequence of the poor preservation potential of the thin, fragile, aragonitic shells and also the association with mangrove and organic-rich sediments from estuarine settings. Anatina burdigalensisCossmann & Peyrot, 1909 (122-3 pl. LXIII fig. 34) from the Miocene (Serravallian 13.82–11.63 Mya) of the Aquitaine Basin, France, resembles the living Exolaternula spengleri in shape (Fig. 1G). Fossils resembling the living Exolaternula liautaudi have been recorded as L. limicola from the mid-Miocene of central Japan (Itoigawa et al., 1981, 1982). Crame (1984) reported Laternula spp. from late Neogene (Pliocene?) deposits of the Makran coast, Pakistan, and these samples (in NHMUK) have shapes resembling living L. anatina. An earlier fossil from the Eocene Rio Turbio Formation of Patagonia [mid-Lutetian to mid-Priabonian, 44.6–34 Mya, date from González Estebenet et al. (2014)], described and figured as Laternula sp. by Griffin (1991: fig. 10 1-2), is broadly similar to L. spengleri in shape (Fig. 1H, I). A possible Late Cretaceous (Campanian/Maastrichtian) Laternula sp. has been described from Argentina (Parras & Griffin, 2013); this is more equivocal in attribution but has an umbonal slit and buttress. Further back in time some Mesozoic genera have been assigned to the Laternulidae, namely Anatimya, Cercomya, Plectomya and Platymyoidea (Keen & Cox, 1969) but these appear morphologically distant from living Laternula. History of Laternula in Antarctica Careful re-examination of both reference collections and the literature indicates that there are no bona fide Early Cenozoic representatives of Laternula from the extensive Early Cenozoic fossil record of Antarctica. The Oligocene–Miocene interval is much less complete (Beu, 2009; Beu & Taviani, 2014). The earliest unequivocal record of the genus is that known from the Cockburn Island Formation, which forms part of a complex sequence of glacial and interglacial sediments interbedded with the late Neogene James Ross Island Volcanic Group (JRIVG), north-eastern Antarctic Peveninsula (Smellie, Johnson & Nelson, 2013; Beu & Taviani, 2014). Specimens from the type area of the formation, Cockburn Island (64°12′S, 56°50′W), were assigned to Laternula elliptica by both Soot-Ryen (1952) and Jonkers (1998a), with the only difference being that their maximum size (150 mm+ in length) somewhat exceeded those of the modern form (Fig. 1F). However, in all other respects they are very close to living L. elliptica and we see no need to assign them to a separate taxon. Co-occurring specimens of the large pectinid Austrochlamys anderssoni (Hennig) have been reliably dated at 4.7 Mya by 87Sr/86Sr isotopes, and this age agrees well with that of 4.7–4.9 Mya for underlying basaltic lavas of the JRIVG (40Ar/39Ar dating) (Smellie et al., 2013). The 4.7 Mya age (i.e. earliest Pliocene) for the specimens of L. elliptica from Cockburn Island represents the earliest definitive fossil record of the genus from Antarctica. Within the James Ross Island group there are sparse records of Laternula from younger glacial/interglacial sediments interbedded with the JRIVG (i.e. the Hobbs Glacier Formation and its lateral equivalents). For example, Laternula sp. is noted from the southern end of Sykes Cliffs on the western side of Croft Bay (64°01′S, 57°49′W) (Jonkers, 1998b), and a poorly constrained 40Ar/39Ar age from overlying lavas was resolved to be 2.38 Mya (Smellie et al., 2013). A potentially older Antarctic specimen of Laternula has been recovered from the Battye Glacier Formation, Prince Charles Mountains, East Antarctica (70°48′S, 68°20′E). Although it clearly possesses a buttressed chondrophore and nacreous inner shell layer, it is very incomplete and can only doubtfully be referred to Laternula? sp. (Stilwell, Harwood & Whitehead, 2002: fig. 2m, n). The suggested Middle–Late Miocene age range for the Battye Glacier Formation is based on the associated diatom assemblage. Better preserved material is available from the Sørsdal Formation, Marine Plain, Vestfold Hills, East Antarctica (68°38′S, 78°8′E), and this has been identified as L. elliptica (Quilty et al., 2016). The Sørsdal Formation is dated by diatoms as Early Pliocene, 4.2–4.1 Mya (Quilty et al., 2016). There is an Early Pleistocene (Galasian) record of L. elliptica from the Scallop Hill Formation of McMurdo Sound (78°11′S, 166°58′E) (Speden, 1962; Beu & Taviani, 2014), and widespread evidence for a Late Quaternary to Holocene circum-Antarctic distribution of the species (Pickard, 1985). DISCUSSION The results show clearly that there are two distinct phylogenetic groups of Laternula species: the clade comprising L. spengleri and L. liautaudi with both species possessing a lithodesma, and the larger clade of all the other species where it is lacking in the adult. A lithodesma is present in the majority of anomalodesmatan families including Pandoridae, Lyonsiidae and Clavagellidae, the sister clades to Laternula (Harper, Hide & Morton, 2000; Harper et al., 2006). Thus, its presence in some species is interpreted as a retained plesiomorphic character and its absence in the larger clade as an apomorphic state. Contrary to Savazzi (1990: 100), only three species of Laternula are known to possess a lithodesma in adult shells: L. spengleri, L. liautaudi and L. erythraea (the last not molecularly sampled). Laternula spengleri and L. liautaudi form a robust clade that supports their classification in a distinct genus, Exolaternula, although other shell characters appear similar to Laternula species. Significantly, Sartori (2009) reported and illustrated lithodesmas in juvenile L. elliptica with shell lengths less than c. 12 mm but these become resorbed in larger shells. This ontogenetic loss of a lithodesma has also been reported in some Thraciidae species (Sartori & Ball, 2009). The three known Exolaternula species are distributed today (Fig. 3) along the northern Indian Ocean and Arabian Gulf (E. erythraea), through south-east Asia (E. spengleri), China, Korea and Japan as far north as Peter the Great Bay, Russia (E. liautaudi). Exolaternula liautaudi also occurs as an exotic on the west coast of the USA (Miller et al., 1999). The distribution of E. spengleri touches the very north of Australia, with a single 19th century (NHMUK) record from Port Essington, Northern Territory. The distribution given in Lamprell & Healy (1998) of this species (as L. rostrata) around southern Australia and New South Wales and followed in some ecological studies is erroneous and based on misidentifications. Figure 3. View largeDownload slide Distributional ranges of Exolaternula and Laternula species in the Indo-West Pacific and Southern Oceans. Robinson projection. Red – Exolaternula, blue – Laternula, green – Laternula elliptica. Figure 3. View largeDownload slide Distributional ranges of Exolaternula and Laternula species in the Indo-West Pacific and Southern Oceans. Robinson projection. Red – Exolaternula, blue – Laternula, green – Laternula elliptica. It seems likely that Exolaternula split from the other Laternula in the early Cenozoic with the clade having a different biogeographical history. We suggest that the present distribution of Exolaternula, restricted to the northern Indian Ocean and southern and eastern margins of Asia, reflects a Tethyan origin. The Miocene Anatina burdigalensis from southern France resembles E. spengleri in shell form and we consider it as a species of Exolaternula, the last survivor in western Tethys before the early Miocene closure of the Tethyan Seaway (Harzhauser et al., 2007). Fossils resembling the living Exolaternula liautaudi were present in Japan at least by the mid-Miocene (Itoigawa et al., 1981, 1982). In the Laternula clade the sister position of Laternula elliptica relative to all other species suggests a separation before the diversification of the temperate and tropical species. This is consistent with the scenario that L. elliptica or its precursor was left isolated around Antarctica after the separation and northward movement of Australia with the opening of the Tasman Gateway and onset of the Antarctic Circumpolar Current c. 30 Mya in the early Oligocene (Scher et al., 2015). This final breakup of the Gondwanan–Weddellian Province (Zinsmeister, 1979) would have disrupted larval interchange as Australia progressively moved northwards. Subsequently, as Australia moved into lower latitudes, warmer water species such as L. anatina may have spread into south-east Asia and the northern Indian Ocean while Australia retained a diversity of temperate water endemic species such as L. gracilis, L. creccina and L. tasmanica, or their precursors. The scenario that L. elliptica originated from a southward migration as a more derived taxon (OTT hypothesis; Jablonski et al., 2006, 2013) during a period of polar amelioration can be rejected. A single record from the Pliocene of New Zealand of a fragmentary fossil, Laternula syntheticaMarwick, 1948, with an estimated shell length of 120 mm (later renamed L. laternaLamarck, 1818 by Beu, 2004) was interpreted to have arrived during a warm period. However, the long pallial sinus of this fossil precludes identification as L. laterna (a tropical species), which has a short sinus, and it most closely resembles the south-eastern Australian species, L. gracilis and L. tasmanica. Although it would be desirable to include more samples in the analysis, our results are consistent with an Australian origin for the tropical Laternula. For example, Laternula creccina from temperate southern Australia is a sister species to tropical L. anatina from Papua New Guinea and sub-tropical L. japonica from Japan. Similarly, L. cf. boschasina from Darwin, northern Australia, is a sister species to two tropical species from Singapore and Thailand. Moreover, the diversity of Laternula species around Australia and their wide latitudinal spread compared with other Indo-West Pacific areas is also evidence supporting this idea. Of the Laternula species, L. anatina (Fig. 1E) has the broadest distribution, recorded from Kenya, the Red Sea, the northern Indian Ocean, through south-eastern Asia, northern Australia to Philippines, China and southern Japan. It is also present as a Lessepsian invader into the eastern Mediterranean (Gofas & Zenetos, 2003). Nonetheless, our preliminary molecular results suggest that cryptic species may exist; for example, the frequently synonymized L. japonica is genetically distinct from L. anatina. Other species at lower latitudes have narrower ranges, L. navicula in the northern Indian Ocean, L. boschasina in south-east Asia and L. laterna around northern Australia. Our phylogenetic evidence supports the idea that Laternula elliptica or its precursor was isolated around Antarctica following the split and northward movement of the Australian continent with the opening of the Tasman Gateway and initiation of the Circum-Antarctic Current. Following separation and onset of cooling conditions the species became adapted physiologically to lower temperatures (Peck et al., 2009). Laternula elliptica differs morphologically from congeners in its much larger size, very wide posterior gape, thicker shell (Watson et al., 2012) and prominent periostracum. It also lacks the exterior shell spikes characteristic of all other Laternula species and many other anomalodesmatans (Checa & Harper, 2010). Laternula elliptica is abundant in shallow water around Antarctica particularly at depths of 10–30 m and even intertidally (Waller et al., 2017), with population densities reported up to 65/m2 (Dell, 1990; Zamorano, Duarte & Moreno, 1986). The general lack of durophagous predators (decapod crustaceans and fish) in Antarctic seas (Clarke et al., 2004) could be a contributory factor in its success. By comparison, the lower latitude species of Laternula tend to occupy peripheral marine habitats where predation pressure is probably reduced, such as mangrove fringes (Morton, 1973; Prezant et al., 2008), estuaries with fluctuating salinities (Kang et al., 2006; Kanaya et al., 2008), or locations with elevated salinities such as Shark Bay, Western Australia (Logan & Cebulski, 1970) or the Arabian Gulf (Sheppard et al., 2010). Corroboration of the biogeographical scenarios with a fossil record would be desirable but as already noted the fossil record of Laternula is poor. The only Southern Hemisphere Early Cenozoic occurrence, Laternula sp. from the Eocene Rio Turbio Formation, Santa Cruz Province, Argentina, is part of a still imperfectly known molluscan fauna that does show at least some resemblance to that known from the La Meseta Formation of Seymour Island, north-eastern Antarctic Peninsula (Griffin, 1991). Palaeogeographical reconstructions for the Eocene connection between Tierra del Fuego and the northern tip of the Antarctic Peninsula are complex, but some of the most recent ones, based on new marine geophysical data, place the Rio Turbio basin at a significantly higher palaeolatitude than its present-day position of 51°30′S (Maldonado et al., 2014: fig. 8). It would certainly have been well within Zinsmeister’s (1979, 1982, 1984) Weddellian Province, and Laternula sp. may represent part of the ancestral lineage of L. elliptica. The Rio Turbio Formation does appear to contain a series of distinct sedimentary facies that are missing in the La Meseta Formation, and the two units almost certainly represent slightly different types of shallow marine environment (Griffin, 1991). As a result of recent taxonomic and stratigraphic studies it has been determined that approximately one-third of the 147 gastropod and bivalve species known from the Middle Eocene section of the La Meseta Formation can now be assigned to modern genera (Beu, 2009; Crame et al., 2014). This means that, for at least one key part of the modern Antarctic marine fauna, it was beginning to take shape some 10–15 Mya before the onset of significant global cooling at the Eocene–Oligocene boundary (Zachos, Dickens & Zeebe, 2008). Molecular phylogenetic evidence suggests that the amphipod genus Epimeria, which today forms a species flock in the Southern Ocean, diversified initially in the Middle or Late Eocene (Verheye, Backeljau & d’Udekem d’Acoz, 2017), and the split between the Antarctic/subantarctic limpet Nacella and its temperate to tropical sister taxon Cellana occurred at 32 Mya (González-Wevar et al., 2017). There is even a combination of molecular phylogenetic and biogeographical evidence from the Antarctic terrestrial realm to suggest that a range of taxa had similar Early Cenozoic roots, and have survived to the present day using various types of refugia (Convey et al., 2008). All of this evidence suggests that the Antarctic biota is of considerable ancestry and has been able to adapt to progressive global cooling over a period of tens of millions of years. Laternula had Eocene or even earlier roots in the Antarctic region and was then able to adapt to both the cooling of Antarctica and the warming of the Australian continent as it moved progressively northwards. Despite the present-day diversity and abundance of Laternula species around Australia, the fossil record from there is lacking, with no mention of the genus in Darragh’s (1985) analysis of the Cenozoic molluscan faunas of south-eastern Australia. However, the stratigraphic record is very patchy and suitable facies are not preserved. Coupled with the preferred marginal marine habitats and fragile shells, this may account for the lack of Laternula fossils. However, Pufahl et al. (2004) report Laternula sp. from Pliocene estuarine deposits in the Murray Basin, South Australia. The fossils are preserved as casts and moulds with aragonitic shells dissolved away and identifications were made in the field (N. James, personal communication). If confirmed, these are the only Laternula fossils recorded from Australia. In summary, our molecular results revealed two distinct groups of living Laternulidae. One comprises Exolaternula species possessing a lithodesma and a distribution largely around the northern Indian Ocean and the southern margin of the Asian continent. The Exolaternula clade probably had a Tethyan origin with connections to the western Tethys in the early Miocene but later severed by the closure of the Tethyan Seaway. The more numerous Laternula species lack a lithodesma in the adult, with the Antarctic L. elliptica as a sister taxon to all other species from Australia and central Indo-West Pacific. The Laternula clade probably originated on the Late Gondwanan southern Australia/Antarctica continent, leaving L. elliptica isolated around Antarctica after Australia split and drifted northwards with opening of the Southern Ocean. Temperate and tropical species exist around Australia but we suggest that the tropical species spread and diversified into coastal Asia from the mid-Miocene onwards after the closer approach of Australia. ACKNOWLEGEMENTS For generously providing samples we are grateful to Ruytoro Goto (University of Kyoto), Barbara Buge (MNHN), Konstatin Lutaenko (Russian Academy of Sciences, Vladivostok), Koh Siang Tan (National University of Singapore), Piotr Kuklinski (Institute of Oceanology, Polish Academy of Sciences) and Simon Morley (BAS). Dawn Woods, George Mulvaney and Michael Mulvaney helped collect samples at Burrill Lake, New South Wales. Grateful thanks are due to Tom Schiotte (NHMD) for images of the Mya anserifera holotype, Emmanuel Tardy (MHNG) for images of the lectotype of Anatina laterna, Virginie Héros (MNHN) for arranging opening of valves and images of the holotype of Laternula liautaudi, Konstantin Lutaenko and Elena Chaban (Zoological Museum, St Petersburg) for searching for the type of L. japonica, and Lisa Kirkendale (WAM) and Richard Willan (MAGNT) for images of shells in their collections. David Cothran generously allowed reproduction of his images of living L. elliptica. Tom Darragh (Museum Victoria) advised on Australian fossil faunas, Pierre Lozouet (MNHN) confirmed dating of fossils and Takuma Haga (NMNS, Tokyo) provided information and literature concerning Japanese living and fossil species. We thank Lisa Smith (NHMUK) for help with molecular analyses and Adrian Glover (NHMUK) who facilitated the process. JAC acknowledges financial support from NERC, including NE/I00582X/1. 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APPENDIX Critical assessment of the living species of Laternulidae and their synonyms. Type localities are given where known. Note that the number of considered valid species and nomenclature differs from Huber (2010) and WoRMS. This classification will evolve as more samples are included in molecular analyses. Laternulidae Genus ExolaternulaHabe, 1977 type species: Anatina truncataLamarck, 1818 = L. spengleri (Gmelin, 1792) = L. rostrata (Sowerby, 1839). Lithodesma present. Exolaternula spengleri(Gmelin, 1792) Solen spengleriGmelin, 1792: 3228. Synonyms: Mya anseriferaSpengler, 1793: table 2, fig. 8, holotype NHMD 116367 (Gmelin’s name is based on this specimen and figure), Nicobar Islands; Anatina truncata auct. non Lamarck 1818; Anatina rostrata (G.B. Sowerby II 1839); Anatina limicolaReeve, 1863, Japan; Anatina elegansPhilippi, 1844, China; Anatina berniculaLamy, 1934, Tongatabu. Remarks: Reeve, (1860) used the name A. anserifera for a figured specimen from Tasmania now considered to be Laternula tasmanica, leading to citations of the former in southern Australia (e.g. Morton, 1976). Distribution: Sri Lanka, Southeast Asia, northern Australia, Philippines, China, southern Japan (Ryukyu Islands). Exolaternula liautaudi (Mittre, 1844) Anatina liautaudiMittre, 1844:16, pl. 104, holotype MNHN-IM- 2000-33234. Manila, Philippines. Image: https://science.mnhn.fr/institution/mnhn/collection/im/item/2000-33234 Synonyms: Laternula limicola auct. non Reeve, 1863; L. navicula auct. non Reeve, 1863; L. marilina auct. non Reeve, 1860; L. gracilis auct. non Reeve, 1860; Anatina kamakuranaPilsbry, 1895, Kamakura, Japan; Anatina pechiliensisGrabau & King, 1928, Peitaiho, NW China; Laternula nanhaiensisZhuang & Cai, 1982, Hepu, Guangxi. Remarks: There has been much nomenclatural confusion concerning this species; in Japanese, Chinese and Russian literature it is often cited as L. marilina, an Australian species lacking a lithodesma and now synonymized with L. gracilis. Comparison of type specimens shows that L. liautaudi, originally described from the Philippines, is the earliest name. Distribution: Northern Philippines, China, Taiwan, Korea, Japan and eastern Russia (Peter the Great Bay), exotic to north-west America. Exolaternula erythraea (Morris & Morris, 1993) Laternula (Exolaternula) erythraeaMorris & Morris, 1993: 8, 19, holotype NHMUK 1992175, Fujairah, United Arab Emirates. Remarks: L. erythraensis was used in error for L. erythraea (e.g. Oliver, 1995; Feulner & Hornby, 2006). Distribution: Arabian Gulf, Gulf of Oman. Genus LaternulaRöding, 1798, type species: Solen anatinusLinnaeus, 1758. Synonym: LaternulinaHabe 1952, type species Anatina japonicaLischke, 1872. Lithodesma absent in adult. Laternula anatina (Linnaeus, 1758) Solen anatinusLinnaeus 1758: 673. Synonyms: Anatina subrostrataLamarck, 1818; Anatina hispidulaCuvier, 1829; Anatina amphoraReeve, 1863, Island of Burias, Philippines; Anatina cumingiReeve, 1863, Amboina; Anatina eximiaReeve, 1863; Anatina flexuosaReeve, 1863, Japan; Anatina labiataReeve, 1863, Ceylon; Anatina siphonataReeve, 1863, Borneo. Remarks: No type material for S. anatinus exists. Linnaeus based the name on the figure in Rumphius (1705: pl. 45 f O and subsequent editions) with locality given as ‘O. Asiatici’. The figure is poor but has the upturned posterior ‘beak’ of shells identified as this species. It is also figured in Chemnitz (1782: 62, pl. 6, figs 46–48) and according to Lamy (1934),Lamarck (1818) based his name A. subrostrata on these figures. Distribution: East Africa (rare), Red Sea, SE Asia, NW Australia, Philippines, China, Okinawa, southern Japan. Exotic to eastern Mediterranean. Laternula elliptica (King, 1832) Anatina ellipticaKing, 1832: 335, holotype NHMUK 197528, South Shetland Islands. Synonym: Anatina prismaticaSowerby, 1834, South Shetland Islands. Remarks: Usually cited as described by Broderip & King (1832) but see Coan, Petit & Zelaya (2011) for authorship. Distribution: Circum-Antarctica, Kerguelen, South Georgia, South Shetland Islands. Laternula boschasina (Reeve, 1860) Anatina boschasinaReeve, 1860, pl. 2, fig. 13, syntypes NHMUK 197513/1–3, Negros Island, Philippines. Remarks: Our sequenced species from Darwin is much smaller than the syntypes but has a similar deep sinus, commarginal folds and brown periostracal margin. Distribution: Uncertain but includes south-east Asia and northern Australia. Laternula bullata (Reeve, 1863) Anatina bullataReeve, 1863, pl. 1 fig. 3, syntypes NHMUK 197513/1–3, Sibonga, Zebu, Philippines. Remarks: The species sequenced from Singapore (sometimes called L. boschasina) is similar to the type with a rounded anterior, tapering posterior and shallow pallial sinus. Distribution: Southeast Asia. Laternula corrugata (Reeve, 1863) Anatina corrugataReeve, 1863, pl. 4, fig. 25, NHMUK 197523/1–2, Ticao Island, Philippines. Remarks: The species sequenced from Shark Bay, Western Australia, is broadly similar to syntypes of this species but may be distinct. Distribution: Philippines, ?Western Australia. Laternula creccina (Reeve, 1860) Anatina creccinaReeve, 1860, pl. 2 fig. 12, NHMUK 197512/1–2, Adelaide, Australia. Synonyms: Anatina vaginaReeve, 1863, Moreton Bay, Australia; Anatina attenuataReeve, 1863, Sydney, Australia. Remarks: The Moreton Bay locality for A. vagina is probably erroneous. Distribution: South-eastern, southern and south-western Australia. Laternula gracilis (Reeve, 1860) Anatina gracilisReeve, 1860, pl. 2 fig. 9, NHMUK 19759/1–3, Moreton Bay, Queensland. Synonyms: Anatina marilinaReeve, 1860, Australia; Anatina rectaReeve, 1863, Port Phillip, Victoria, Australia; ?Anatina tasmanicaReeve, 1863, Tasmania. Remarks: Molecular analysis indicates that specimens identified as three species above are monospecific with L. gracilis taking priority. The status of the largest species, L. tasmanica, is uncertain but shares characters with L. gracilis. Distribution: Eastern Australia from southern Queensland to Victoria and Tasmania. Laternula impura (Pilsbry 1901) Anatina impuraPilsbry, 1901: 208, pl. 19 fig. 9, syntypes ANSP 68536, Sagami, Japan. Remarks: The status of this species is uncertain. Distribution: Southern Japan Laternula japonicaLischke, 1872: 107; fig. 1874, pl. 9, figs 7–10, types not located, Tokyo, Japan. Remarks: This species is often synonymized with L. anatina but our molecular results indicate it is genetically distinct. An earlier name may be Anatina blainvilleiReeve, 1863, pl. 3, fig 17, Island of Burias, Philippines. Distribution: Southern Japan. Laternula laterna (Lamarck, 1818) Anatina laternaLamarck 1818: 463, lectotype MNHG 1082/33 selected Beu (2004: 184, fig. 18C–E). Synonyms: Anatina cistellaReeve, 1863, Moluccas; Anatina constricta, Reeve, 1863, northern Australia; A. valenciennesiiReeve, 1863, China. Remarks: The lectotype is a large specimen with a short posterior beak and differs from the Lamarckian syntype specimens (now paralectotypes) labelled A. laterna in MNHN Paris (Lamy, 1934, pl. 1, fig. 7). Distribution: Northern Australia, Indonesia. Beu (2004) wrongly states, citing Lamprell & Healy (1998: 214), that the distribution ranges from southern Western Australia to South Australia, Victoria, Tasmania and New South Wales. Laternula navicula (Reeve, 1863) Anatina naviculaReeve, 1863, pl. 4 fig. 21, NHMUK 197520/1–3, type locality not cited. Synonyms: Anatina barkudaensis Preston, 1915, Lake Chilka, India; Anatina barkulensisPreston, 1915, Lake Chilka; Anatina granulosaPreston, 1914, Lake Chilka; Anatina smithiPreston, 1905, Sri Lanka. Distribution: NW Indian Ocean, Arabian Sea, India, Sri Lanka, Andaman Sea. Laternula sp. Remarks: This species, collected in Kungkraben Bay, Thailand, and called L. corrugata by Prezant et al. (2008) and then changed to L. anatinaPrezant et al. (2015), is neither of these taxa. It is broadly similar in shape to L. bullataReeve, 1860 but molecularly distinct from Singapore specimens that we identify as that species. The following species are of uncertain status; all are small shells and probably juveniles. Anatina fabaReeve, 1863, pl. 4, fig. 22, Brisbane, type not located. Anatina argenteaReeve, 1863, pl. 4, fig. 29, NHMUK 197526. Anatina prolongataReeve, 1863, pl. 4, fig. 28, Port Curtis, Queensland, type not located. © 2018 The Linnean Society of London, Biological Journal of the Linnean Society

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