TY - JOUR
AU - Marian, José Eduardo A, R
AB - Abstract One of the most intriguing puzzles in macroevolutionary studies is to understand how distantly related taxa can evolve towards similar phenotypes in response to similar ecological conditions. Ark clams and their relatives (Arcida) display two main ecologies represented by epifaunal and infaunal lifestyles. Their mantle margin includes features, such as photosensory and muscular organs, that may coincide with each habit, making these bivalves a suitable model to explore evolutionary convergence in the marine benthos. To test for the evolutionary association between lifestyles and morphology, we gathered data on the mantle margin for 64 species across all six extant arcidan families. A molecular phylogeny of Arcida was inferred based on four gene sequences from 54 species and used to study trait evolution. Our results support the hypothesis that photoreceptor organs had a single origin and that infaunal lineages lost these structures in independent events, suggesting a correlated pattern of evolution. In addition, the enlargement of the posterior inner fold, which acts as a functional siphon, favoured the occurrence of convergent transitions to infaunal habits during the Mesozoic. We provide evidence of ecomorphological associations and putative adaptations in a bivalve clade that sheds light on the underlying factors driving evolution of the marine benthos. adaptation, correlation, lifestyle, mantle, phenotype, phylogeny INTRODUCTION Macroevolutionary questions compose the core of evolutionary biology and focus on the association of phenotypical diversity with adaptive landscapes (Simpson, 1953; Schluter, 2000). Understanding whether and how similar ecological factors can drive independent taxa towards the same phenotype may help us to understand the factors that drive evolution better (Losos, 2011; Serb et al., 2017). In this context, the repeated evolution of traits across independent lineages, i.e. evolutionary convergence (Agrawal, 2017), in association with similar environmental factors suggests putative adaptations and predictable responses to similar selective regimes (Harvey & Pagel, 1991; Losos, 2011; Mahler et al., 2017). Numerous vertebrate taxa are used as models for studies on evolutionary processes and convergence (Losos & Mahler, 2010), whereas invertebrates are proportionally less studied, and supposed ecomorphological patterns in invertebrate taxa remain largely obscure. Ark clams and their relatives (Bivalvia, Arcida) are marine pteriomorphian bivalves and are a suitable model to gain insights into convergent evolution owing to their morphological and ecological diversity. Two main lifestyles are observed in the group (Oliver & Holmes, 2006). Epifaunal animals are attached to hard substrate (e.g. rocks and coral fragments) by a strong byssus (i.e. filaments secreted to attach the animal to solid surfaces). Alternatively, infaunal and semi-infaunal animals bury into soft sediment, leaving the posterior region exposed above the surface. Previous anatomical studies have identified apparent associations between both modes of life with putative adaptations of shell shape, muscle organization and photoreceptor organs (Stanley, 1972; Oliver & Holmes, 2006; Audino & Marian, 2018); however, these hypotheses were not tested directly using comparative methods. The Arcida Gray, 1854 have a comprehensive fossil record dating back to the lower Ordovician (~450 Mya; Morton et al., 1998; Cope, 2000). The Order currently encompasses the superfamilies Arcoidea and Limopsoidea, with an estimated diversity of > 300 extant species (Oliver & Holmes, 2006; Carter et al., 2011). The Arcoidea traditionally includes the families Arcidae, Cucullaeidae, Noetiidae and Glycymerididae, whereas Limopsidae and Philobryidae are assigned to Limopsoidea (Oliver & Holmes, 2006; Carter et al., 2011). Nevertheless, taxonomic classifications are controversial, with numerous morphological features that are likely to represent homoplasies in response to similar ecologies (Oliver & Holmes, 2006). One of these features is the mantle margin, a narrow region of soft tissues organized as lobe-like extensions lining the shell margin (Fig. 1A, B). This region is expected to evolve in response to shifts in lifestyle given that the mantle margin plays primary roles of interaction with the surrounding environment, including sensory, protective and muscular functions (Yonge, 1983; Audino & Marian, 2016). The siphons are a classical example of a key morphological innovation in infaunal bivalves as a result of enlargement and fusion of the mantle folds. Siphons create channels for water circulation through the mantle cavity, where the gills are located, in animals that live constantly buried within the sediment (Yonge, 1983; Stanley, 1968). Other mantle structures, such as eyes and tentacles, have also been linked to ecological transitions. For instance, in scallops, depth was suggested to be an important driving force in the evolution of mantle eye components associated with light sensitivity (Malkowsky & Götze, 2014). Light-guided behaviours, e.g. related to predator detection and posture control (Nilsson, 1994), could also be associated with transitions to the epifaunal habit, i.e. when the animal lives on top of the substrate. Consequently, the mantle margin in Arcida represents a promising source of information to identify convergent traits and test correlated evolution. Phenotypic diversity in the number and length of mantle folds and in the presence and complexity of photoreceptor organs are among key traits of this region (Waller, 1980; Morton, 1982; Morton & Peharda, 2008; Audino & Marian, 2018). Nevertheless, the structure of the mantle margin in the ancestor of ark clams and its subsequent morphological diversification have never been inferred, rendering several interesting questions. For example, did photoreceptor organs of the mantle margin evolve as adaptive traits in epifaunal groups? Are changes in mantle morphology related to shifts to the infaunal lifestyle? For instance, the enlarged posterior mantle fold of infaunal lineages may act as a functional siphon (e.g. Morton, 1982); did this attribute evolve convergently as an adaptation (or exaptation; Gould & Vrba, 1982) to the infaunal lifestyle? Figure 1. View largeDownload slide General organization of the mantle (A) and mantle margin (B) in Arcida represented by simplified schemes. Mantle margin morphology in Arcidae (C–E, G–N) and Cucullaeidae (F). Posterior mantle region, ventral view. Scale bars: 1 mm. The first outer fold can be pigmented (C–G), bearing multiple compound eyes (arrows) and pigmented eyespots (arrowheads). The middle fold is reduced (E) or absent (J). The inner fold is much longer than the other folds, forming a large curtain (I–N) or a posterior flap (M). C, Acar plicata (USNM 886349). D, Arca noae (USNM 1086014). E, Barbatia fusca (SBMNH 349329). F, Cucullaea labiata (USNM 746883). G, Barbatia barbata (MCZ 378867). H, Barbatia virescens (MCZ 378874). I, Barbatia candida (MZSP 105572). J, Anadara broughtonii (USNM 802331). K, Anadara ferruginea (SBMNH 81002). L, Tegillarca granosa (MCZ 378820). M, Bathyarca corpulenta (SBMNH 349320). N, Trisidos kiyonoi (SBMNH 97422). Abbreviations: aa, anterior adductor; if, inner fold; ma, mantle; mf, middle fold; mm, mantle margin; of, outer fold; of-1, first outer fold; of-2, second outer fold; pa, posterior adductor; pe, pigmented eyespots; pg, periostracal groove; sh, shell. Figure 1. View largeDownload slide General organization of the mantle (A) and mantle margin (B) in Arcida represented by simplified schemes. Mantle margin morphology in Arcidae (C–E, G–N) and Cucullaeidae (F). Posterior mantle region, ventral view. Scale bars: 1 mm. The first outer fold can be pigmented (C–G), bearing multiple compound eyes (arrows) and pigmented eyespots (arrowheads). The middle fold is reduced (E) or absent (J). The inner fold is much longer than the other folds, forming a large curtain (I–N) or a posterior flap (M). C, Acar plicata (USNM 886349). D, Arca noae (USNM 1086014). E, Barbatia fusca (SBMNH 349329). F, Cucullaea labiata (USNM 746883). G, Barbatia barbata (MCZ 378867). H, Barbatia virescens (MCZ 378874). I, Barbatia candida (MZSP 105572). J, Anadara broughtonii (USNM 802331). K, Anadara ferruginea (SBMNH 81002). L, Tegillarca granosa (MCZ 378820). M, Bathyarca corpulenta (SBMNH 349320). N, Trisidos kiyonoi (SBMNH 97422). Abbreviations: aa, anterior adductor; if, inner fold; ma, mantle; mf, middle fold; mm, mantle margin; of, outer fold; of-1, first outer fold; of-2, second outer fold; pa, posterior adductor; pe, pigmented eyespots; pg, periostracal groove; sh, shell. A phylogenetic framework is crucial to provide initial steps towards these answers and elucidate the number of ecological transitions in the clade. Although the Arcida has been recovered monophyletic in many analyses (Steiner & Hammer, 2000; Giribet & Wheeler, 2002; Matsumoto, 2003; Bieler et al., 2014), relationships among families and superfamilies remain under debate (Oliver & Holmes, 2006; Bieler et al., 2014; Feng et al., 2015; Combosch & Giribet, 2016). The placement of some groups, such as the Glycymerididae and the Limopsoidea, is particularly challenging (Combosch & Giribet, 2016). Consequently, a more robust phylogeny is needed to enable further evolutionary studies on the radiation of the group. The present study provides the most comprehensive phylogenetic analysis of Arcida to investigate morphological evolution in the clade and cast light on presumed adaptive features. Particularly, mantle margin morphology and lifestyles were studied in 64 species under a phylogenetic framework to test for correlation between lifestyle and morphology. The inferred molecular phylogenies, combined with the extensive morphological survey, provided a robust basis for discussion of evolutionary patterns in the clade. MATERIAL AND METHODS Taxa sampling Nucleotide sequences for four genes (18S rRNA, 28S rRNA, COI mtDNA and histone H3) were obtained from GenBank for 54 species of Arcida, covering both superfamilies, all six families and 20 genera (Table 1). The outgroup comprised seven species from other pteriomorphian orders and five species from the remaining major bivalve clades (Protobranchia and Heteroconchia) (Table 1). Missing data corresponded to 12% of the dataset for nucleotide sequences (Table 1). When possible, sampling effort was proportional to the diversity of each family, i.e. relatively more samples were analysed in groups that were comparatively more diverse (Table 1). Table 1. Taxa included in the phylogenetic and morphological analyses Taxa Reference 18S rRNA 28S rRNA COI mtDNA Histone H3 Collections Arcidae Acar dominguensis (Lamarck, 1819) FJ480593 KT757861 MZSP118292 Acar gradata (Broderip & Sowerby I, 1829) USNM796185 Acar plicata (Dillwyn, 1817) AJ389630 AJ307533 FJ480453 AF416856 MZSP115322 Anadara antiquata (Linnaeus, 1758) JN974491 JN974542 HQ258850 JN974592 MZSP99848 Anadara baughmani Hertlein, 1951 USNM803522 Anadara broughtonii (Schrenck, 1867) JN974489 JN974541 HQ258847 JN974590 USNM802331 Anadara chemnitzii (Philippi, 1851) MZSP43259, ZUECBIV4870 Anadara cornea (Reeve, 1844) JN974499 DQ343860 HQ258856 JN974600 Anadara crebricostata (Reeve, 1844) JN974495 JN974547 HQ258859 JN974596 Anadara ferruginea (Reeve, 1944) SBMNH81002 Anadara floridana (Conrad, 1869) USNM847847 Anadara globosa (Reeve, 1844) JN974484 JN974535 HQ258861 JN974584 Anadara grandis (Broderip & Sowerby I, 1829) USNM803487 Anadara gubernaculum (Reeve, 1844) JN974493 JN974544 HQ258857 JN974594 Anadara inaequivalvis (Bruguiere, 1789) JN974497 JN974548 AB076937 JN974598 MZSP55060 Anadara notabilis (Röding, 1798) KT757768 KT757816 AF416828 KT757863 MZSP84987, MZSP84886 Anadara obesa (G. B. Sowerby I, 1833) MCZ337676 Anadara pilula (Reeve, 1843) JN974507 JN974558 HQ258862 JN974608 Anadara subcrenata (Lischle, 1869) JN974501 DQ343861 HQ258851 JN974602 Anadara transversa (Say, 1822) USNM801135, MCZ359001 Anadara trapezia (Deshayes, 1839) KT757770 KT757817 KX713443 KT757865 SBMNH10187 Anadara vellicata (Reeve, 1844) JN974487 JN974539 HQ258848 JN974588 Arca imbricata Bruguière, 1789 AY654986 KT757820 AF253494 AY654989 MZSP95208, MZSP109869 Arca navicularis Bruguière, 1789 JN974517 KT757821 HQ258822 JN974618 USNM719071, MCZ378833 Arca noae Linnaeus, 1758 KC429325 KT757822 KC429090 KC429160 USNM1086014 Arca patriarchalis Röding, 1798 JN974527 JN974576 JN974627 MZSP99765 Arca ventricosa (Lamarck, 1819) AB076935 AF416854 MZSP55027 Arca zebra (Swainson, 1833) KT757776 KT757824 AF416864 MZSP101688 Barbatia amygdalumtostum (Röding, 1798) JN974526 JN974575 JN974626 SBMNH349329, USNM847011 Barbatia barbata (Linnaeus, 1758) KC429326 KT757825 KC429091 KC429161 MCZ378867 Barbatia cancellaria (Lamarck, 1819) KT757779 KT757827 MZSP32336, MZSP48857 Barbatia candida (Helbling, 1779) KT757784 KT757831 AF253487 AF416849 MZSP105572, ZUECBIV1407 Barbatia lacerata (Bruguière, 1789) JN974509 JN974560 HQ258826 JN974610 Barbatia lima (Reeve, 1844) JN974511 JN974563 HQ258837 JN974612 MZSP71135 Barbatia virescens (Reeve, 1844) JN974524 KT757835 HQ258840 JN974624 MZSP71367, MCZ378874 Bathyarca corpulenta (E. A. Smith, 1885) SBMNH349320 Bathyarca glomerula (Dall, 1881) KT757790 KT757837 KT757880 Bathyarca pectunculoides (Scacchi, 1835) MCZ348402 Bentharca asperula (Dall, 1881) MCZ348399 Lunarca ovalis (Bruguière, 1789) GQ166571 AF416844 MZSP84823, USNM803532 Tegillarca granosa (Linnaeus, 1758) JN974505 KT757857 HQ258867 JN974606 MZSP55596, MCZ378820 Tegillarca nodifera (Martens, 1860) JN974503 JN974554 HQ258869 JN974604 Trisidos kiyonoi (Makiyama, 1931) JN974522 JN974571 HQ258846 JN974622 SBMNH97422, SBMNH97423 Trisidos tortuosa (Linnaeus, 1758) KT757811 KT757858 KT757899 Cucullaeidae Cucullaea labiata (Lightfoot, 1786) JN974513 JN974565 KJ774477 JN974614 USNM746883 Noetiidae Arcopsis adamsi (Dall, 1886) KC429327 KC429419 KC429092 KC429162 MZSP19724, ZUECBIV1153 Didimacar tenebrica (Reeve, 1844) JN974515 JN974566 HQ258870 JN974616 SBMNH80722 Eontia ponderosa (Say, 1822) KT757793 KT757840 AF416834 AF416860 SBMNH235066, USNM803530 Sheldonella bisulcata (Lamarck, 1819) MZSP26911 Striarca lactea (Linnaeus, 1758) AF120531 KT757855 AF120646 USNM857645, MCZ379156 Striarca symmetrica (Reeve, 1844) MZSP55574 Glycymerididae Glycymeris decussata (Linnaeus, 1758) MZSP91966 Glycymeris gigantea (Reeve, 1843) KT757794 KT757841 KT757883 MCZ 378989 Glycymeris glycymeris (Linnaeus, 1758) KC429328 KC429421 KC429093 KC429163 USNM794960 Glycymeris holoserica (Reeve, 1843) KT757796 KT757843 KT757885 MCZ378984 Glycymeris longior (G. B. Sowerby, 1833) MZSP91201, ZUECBIV78 Glycymeris nummaria (Linnaeus, 1758) KT757798 KT757845 KX785178 KT757887 MCZ378985 Glycymeris septentrionalis (Middendorff, 1849) KT757799 KT757846 KF643645 KT757888 Glycymeris tenuicostata (Reeve, 1843) KT757800 KT757847 KT757889 MCZ378982 Glycymeris undata (Linnaeus, 1758) MZSP91983 Tucetona pectinata (Gmelin, 1791) KT757812 KT757859 KX713507 KT757900 MZSP91971, ZUECBIV2198 Limopsidae Limopsis aurita (Brocchi, 1814) ZUECBIV2248, MCZ348438 Limopsis cristata Jeffreys, 1876 MZSP104154, MCZ348410 Limopsis cumingi Adams, 1863 KT757802 AB076930 Limopsis enderbyensis Powell, 1958 AJ422057 AY321301 Limopsis galatheae Knudsen, 1970 MCZ348437 Limopsis lilliei E. A. Smith, 1915 MZSP90647, USNM904585 Limopsis marionensis E. A. Smith, 1885 AJ422058 AY321303 USNM760835, USNM886526 Limopsis sp. Sassi, 1827 KC429329 KC429422 KC429164 Limopsis sulcata Verrill & Bush, 1898 USNM832925 Limopsis tenella Jeffreys, 1876 USNM807040 Philobryidae Adacnarca nitens Pelseneer, 1903 KP340836 KT757815 KT757862 MZSP90616, USNM886551 Lissarca notorcardensis Melvill & Standen, 1907 EF192520 KF612434 MZSP87826, USNM899485 Neocardia sp. G. B. Sowerby III, 1892 KT757804 KT757850 KX713486 KT757891 USNM881121, MCZ378927 Philobrya magellanica (Stempell, 1899) KP340845 KT757853 KT757895 Philobrya sublaevis Pelseneer, 1903 KP340835 KP340812 MZSP90645, USNM882353 Outgroup: Pteriomorphia Lima lima (Linnaeus, 1758) KC429339 KC429434 KC429101 KC429174 USNM 754383 Malleus albus Lamarck, 1819 KC429334 HQ329464 KC429097 KC429169 MZSP55595 Mytilus edulis Linnaeus, 1758 KC429331 KC429424 KF644190 KC429166 MZSP120321 Ostrea edulis Linnaeus, 1758 L49052 AF137047 AF120651 AY070151 USNM836256 Pecten maximus (Linnaeus, 1758) L49053 HM630545 KC429102 EU379508 Pinctada margaritifera (Linnaeus, 1758) AB214451 AB214466 AB259166 HQ329296 USNM836493 Pinna carnea Gmelin, 1791 HQ329375 KJ366067 KJ366325 KC429172 MZSP29040 Outgroup: Bivalvia Chione elevata (Say, 1822) KC429387 KC429495 KC429136 KC429219 Macoma balthica (Linnaeus, 1758) KC429393 KC429501 KC429141 KC429224 Margaritifera margaritifera (Linnaeus, 1758) AF229612 KC429443 AF303316 KC429185 Neotrigonia lamarckii (Gray, 1838) KC429345 KC429443 KC429105 KC429182 Nucula sulcuta Bronn, 1831 AF207642 KC984815 KC984746 KC984777 Taxa Reference 18S rRNA 28S rRNA COI mtDNA Histone H3 Collections Arcidae Acar dominguensis (Lamarck, 1819) FJ480593 KT757861 MZSP118292 Acar gradata (Broderip & Sowerby I, 1829) USNM796185 Acar plicata (Dillwyn, 1817) AJ389630 AJ307533 FJ480453 AF416856 MZSP115322 Anadara antiquata (Linnaeus, 1758) JN974491 JN974542 HQ258850 JN974592 MZSP99848 Anadara baughmani Hertlein, 1951 USNM803522 Anadara broughtonii (Schrenck, 1867) JN974489 JN974541 HQ258847 JN974590 USNM802331 Anadara chemnitzii (Philippi, 1851) MZSP43259, ZUECBIV4870 Anadara cornea (Reeve, 1844) JN974499 DQ343860 HQ258856 JN974600 Anadara crebricostata (Reeve, 1844) JN974495 JN974547 HQ258859 JN974596 Anadara ferruginea (Reeve, 1944) SBMNH81002 Anadara floridana (Conrad, 1869) USNM847847 Anadara globosa (Reeve, 1844) JN974484 JN974535 HQ258861 JN974584 Anadara grandis (Broderip & Sowerby I, 1829) USNM803487 Anadara gubernaculum (Reeve, 1844) JN974493 JN974544 HQ258857 JN974594 Anadara inaequivalvis (Bruguiere, 1789) JN974497 JN974548 AB076937 JN974598 MZSP55060 Anadara notabilis (Röding, 1798) KT757768 KT757816 AF416828 KT757863 MZSP84987, MZSP84886 Anadara obesa (G. B. Sowerby I, 1833) MCZ337676 Anadara pilula (Reeve, 1843) JN974507 JN974558 HQ258862 JN974608 Anadara subcrenata (Lischle, 1869) JN974501 DQ343861 HQ258851 JN974602 Anadara transversa (Say, 1822) USNM801135, MCZ359001 Anadara trapezia (Deshayes, 1839) KT757770 KT757817 KX713443 KT757865 SBMNH10187 Anadara vellicata (Reeve, 1844) JN974487 JN974539 HQ258848 JN974588 Arca imbricata Bruguière, 1789 AY654986 KT757820 AF253494 AY654989 MZSP95208, MZSP109869 Arca navicularis Bruguière, 1789 JN974517 KT757821 HQ258822 JN974618 USNM719071, MCZ378833 Arca noae Linnaeus, 1758 KC429325 KT757822 KC429090 KC429160 USNM1086014 Arca patriarchalis Röding, 1798 JN974527 JN974576 JN974627 MZSP99765 Arca ventricosa (Lamarck, 1819) AB076935 AF416854 MZSP55027 Arca zebra (Swainson, 1833) KT757776 KT757824 AF416864 MZSP101688 Barbatia amygdalumtostum (Röding, 1798) JN974526 JN974575 JN974626 SBMNH349329, USNM847011 Barbatia barbata (Linnaeus, 1758) KC429326 KT757825 KC429091 KC429161 MCZ378867 Barbatia cancellaria (Lamarck, 1819) KT757779 KT757827 MZSP32336, MZSP48857 Barbatia candida (Helbling, 1779) KT757784 KT757831 AF253487 AF416849 MZSP105572, ZUECBIV1407 Barbatia lacerata (Bruguière, 1789) JN974509 JN974560 HQ258826 JN974610 Barbatia lima (Reeve, 1844) JN974511 JN974563 HQ258837 JN974612 MZSP71135 Barbatia virescens (Reeve, 1844) JN974524 KT757835 HQ258840 JN974624 MZSP71367, MCZ378874 Bathyarca corpulenta (E. A. Smith, 1885) SBMNH349320 Bathyarca glomerula (Dall, 1881) KT757790 KT757837 KT757880 Bathyarca pectunculoides (Scacchi, 1835) MCZ348402 Bentharca asperula (Dall, 1881) MCZ348399 Lunarca ovalis (Bruguière, 1789) GQ166571 AF416844 MZSP84823, USNM803532 Tegillarca granosa (Linnaeus, 1758) JN974505 KT757857 HQ258867 JN974606 MZSP55596, MCZ378820 Tegillarca nodifera (Martens, 1860) JN974503 JN974554 HQ258869 JN974604 Trisidos kiyonoi (Makiyama, 1931) JN974522 JN974571 HQ258846 JN974622 SBMNH97422, SBMNH97423 Trisidos tortuosa (Linnaeus, 1758) KT757811 KT757858 KT757899 Cucullaeidae Cucullaea labiata (Lightfoot, 1786) JN974513 JN974565 KJ774477 JN974614 USNM746883 Noetiidae Arcopsis adamsi (Dall, 1886) KC429327 KC429419 KC429092 KC429162 MZSP19724, ZUECBIV1153 Didimacar tenebrica (Reeve, 1844) JN974515 JN974566 HQ258870 JN974616 SBMNH80722 Eontia ponderosa (Say, 1822) KT757793 KT757840 AF416834 AF416860 SBMNH235066, USNM803530 Sheldonella bisulcata (Lamarck, 1819) MZSP26911 Striarca lactea (Linnaeus, 1758) AF120531 KT757855 AF120646 USNM857645, MCZ379156 Striarca symmetrica (Reeve, 1844) MZSP55574 Glycymerididae Glycymeris decussata (Linnaeus, 1758) MZSP91966 Glycymeris gigantea (Reeve, 1843) KT757794 KT757841 KT757883 MCZ 378989 Glycymeris glycymeris (Linnaeus, 1758) KC429328 KC429421 KC429093 KC429163 USNM794960 Glycymeris holoserica (Reeve, 1843) KT757796 KT757843 KT757885 MCZ378984 Glycymeris longior (G. B. Sowerby, 1833) MZSP91201, ZUECBIV78 Glycymeris nummaria (Linnaeus, 1758) KT757798 KT757845 KX785178 KT757887 MCZ378985 Glycymeris septentrionalis (Middendorff, 1849) KT757799 KT757846 KF643645 KT757888 Glycymeris tenuicostata (Reeve, 1843) KT757800 KT757847 KT757889 MCZ378982 Glycymeris undata (Linnaeus, 1758) MZSP91983 Tucetona pectinata (Gmelin, 1791) KT757812 KT757859 KX713507 KT757900 MZSP91971, ZUECBIV2198 Limopsidae Limopsis aurita (Brocchi, 1814) ZUECBIV2248, MCZ348438 Limopsis cristata Jeffreys, 1876 MZSP104154, MCZ348410 Limopsis cumingi Adams, 1863 KT757802 AB076930 Limopsis enderbyensis Powell, 1958 AJ422057 AY321301 Limopsis galatheae Knudsen, 1970 MCZ348437 Limopsis lilliei E. A. Smith, 1915 MZSP90647, USNM904585 Limopsis marionensis E. A. Smith, 1885 AJ422058 AY321303 USNM760835, USNM886526 Limopsis sp. Sassi, 1827 KC429329 KC429422 KC429164 Limopsis sulcata Verrill & Bush, 1898 USNM832925 Limopsis tenella Jeffreys, 1876 USNM807040 Philobryidae Adacnarca nitens Pelseneer, 1903 KP340836 KT757815 KT757862 MZSP90616, USNM886551 Lissarca notorcardensis Melvill & Standen, 1907 EF192520 KF612434 MZSP87826, USNM899485 Neocardia sp. G. B. Sowerby III, 1892 KT757804 KT757850 KX713486 KT757891 USNM881121, MCZ378927 Philobrya magellanica (Stempell, 1899) KP340845 KT757853 KT757895 Philobrya sublaevis Pelseneer, 1903 KP340835 KP340812 MZSP90645, USNM882353 Outgroup: Pteriomorphia Lima lima (Linnaeus, 1758) KC429339 KC429434 KC429101 KC429174 USNM 754383 Malleus albus Lamarck, 1819 KC429334 HQ329464 KC429097 KC429169 MZSP55595 Mytilus edulis Linnaeus, 1758 KC429331 KC429424 KF644190 KC429166 MZSP120321 Ostrea edulis Linnaeus, 1758 L49052 AF137047 AF120651 AY070151 USNM836256 Pecten maximus (Linnaeus, 1758) L49053 HM630545 KC429102 EU379508 Pinctada margaritifera (Linnaeus, 1758) AB214451 AB214466 AB259166 HQ329296 USNM836493 Pinna carnea Gmelin, 1791 HQ329375 KJ366067 KJ366325 KC429172 MZSP29040 Outgroup: Bivalvia Chione elevata (Say, 1822) KC429387 KC429495 KC429136 KC429219 Macoma balthica (Linnaeus, 1758) KC429393 KC429501 KC429141 KC429224 Margaritifera margaritifera (Linnaeus, 1758) AF229612 KC429443 AF303316 KC429185 Neotrigonia lamarckii (Gray, 1838) KC429345 KC429443 KC429105 KC429182 Nucula sulcuta Bronn, 1831 AF207642 KC984815 KC984746 KC984777 Nucleotide sequences were obtained in the GenBank database; accession numbers are listed. Morphological investigation was conducted with taxa included in the phylogenetic study (when possible) and additional species; catalogue numbers are indicated. Abbreviations: MCZ, Museum of Comparative Zoology; MZSP, Museum of Zoology of the University of São Paulo; SBMNH, Santa Barbara Museum of Natural History; USNM, Smithsonian National Museum of Natural History; ZUECBIV, Museum of Zoology ‘Prof. Adão José Cardoso’ of the University of Campinas. View Large Table 1. Taxa included in the phylogenetic and morphological analyses Taxa Reference 18S rRNA 28S rRNA COI mtDNA Histone H3 Collections Arcidae Acar dominguensis (Lamarck, 1819) FJ480593 KT757861 MZSP118292 Acar gradata (Broderip & Sowerby I, 1829) USNM796185 Acar plicata (Dillwyn, 1817) AJ389630 AJ307533 FJ480453 AF416856 MZSP115322 Anadara antiquata (Linnaeus, 1758) JN974491 JN974542 HQ258850 JN974592 MZSP99848 Anadara baughmani Hertlein, 1951 USNM803522 Anadara broughtonii (Schrenck, 1867) JN974489 JN974541 HQ258847 JN974590 USNM802331 Anadara chemnitzii (Philippi, 1851) MZSP43259, ZUECBIV4870 Anadara cornea (Reeve, 1844) JN974499 DQ343860 HQ258856 JN974600 Anadara crebricostata (Reeve, 1844) JN974495 JN974547 HQ258859 JN974596 Anadara ferruginea (Reeve, 1944) SBMNH81002 Anadara floridana (Conrad, 1869) USNM847847 Anadara globosa (Reeve, 1844) JN974484 JN974535 HQ258861 JN974584 Anadara grandis (Broderip & Sowerby I, 1829) USNM803487 Anadara gubernaculum (Reeve, 1844) JN974493 JN974544 HQ258857 JN974594 Anadara inaequivalvis (Bruguiere, 1789) JN974497 JN974548 AB076937 JN974598 MZSP55060 Anadara notabilis (Röding, 1798) KT757768 KT757816 AF416828 KT757863 MZSP84987, MZSP84886 Anadara obesa (G. B. Sowerby I, 1833) MCZ337676 Anadara pilula (Reeve, 1843) JN974507 JN974558 HQ258862 JN974608 Anadara subcrenata (Lischle, 1869) JN974501 DQ343861 HQ258851 JN974602 Anadara transversa (Say, 1822) USNM801135, MCZ359001 Anadara trapezia (Deshayes, 1839) KT757770 KT757817 KX713443 KT757865 SBMNH10187 Anadara vellicata (Reeve, 1844) JN974487 JN974539 HQ258848 JN974588 Arca imbricata Bruguière, 1789 AY654986 KT757820 AF253494 AY654989 MZSP95208, MZSP109869 Arca navicularis Bruguière, 1789 JN974517 KT757821 HQ258822 JN974618 USNM719071, MCZ378833 Arca noae Linnaeus, 1758 KC429325 KT757822 KC429090 KC429160 USNM1086014 Arca patriarchalis Röding, 1798 JN974527 JN974576 JN974627 MZSP99765 Arca ventricosa (Lamarck, 1819) AB076935 AF416854 MZSP55027 Arca zebra (Swainson, 1833) KT757776 KT757824 AF416864 MZSP101688 Barbatia amygdalumtostum (Röding, 1798) JN974526 JN974575 JN974626 SBMNH349329, USNM847011 Barbatia barbata (Linnaeus, 1758) KC429326 KT757825 KC429091 KC429161 MCZ378867 Barbatia cancellaria (Lamarck, 1819) KT757779 KT757827 MZSP32336, MZSP48857 Barbatia candida (Helbling, 1779) KT757784 KT757831 AF253487 AF416849 MZSP105572, ZUECBIV1407 Barbatia lacerata (Bruguière, 1789) JN974509 JN974560 HQ258826 JN974610 Barbatia lima (Reeve, 1844) JN974511 JN974563 HQ258837 JN974612 MZSP71135 Barbatia virescens (Reeve, 1844) JN974524 KT757835 HQ258840 JN974624 MZSP71367, MCZ378874 Bathyarca corpulenta (E. A. Smith, 1885) SBMNH349320 Bathyarca glomerula (Dall, 1881) KT757790 KT757837 KT757880 Bathyarca pectunculoides (Scacchi, 1835) MCZ348402 Bentharca asperula (Dall, 1881) MCZ348399 Lunarca ovalis (Bruguière, 1789) GQ166571 AF416844 MZSP84823, USNM803532 Tegillarca granosa (Linnaeus, 1758) JN974505 KT757857 HQ258867 JN974606 MZSP55596, MCZ378820 Tegillarca nodifera (Martens, 1860) JN974503 JN974554 HQ258869 JN974604 Trisidos kiyonoi (Makiyama, 1931) JN974522 JN974571 HQ258846 JN974622 SBMNH97422, SBMNH97423 Trisidos tortuosa (Linnaeus, 1758) KT757811 KT757858 KT757899 Cucullaeidae Cucullaea labiata (Lightfoot, 1786) JN974513 JN974565 KJ774477 JN974614 USNM746883 Noetiidae Arcopsis adamsi (Dall, 1886) KC429327 KC429419 KC429092 KC429162 MZSP19724, ZUECBIV1153 Didimacar tenebrica (Reeve, 1844) JN974515 JN974566 HQ258870 JN974616 SBMNH80722 Eontia ponderosa (Say, 1822) KT757793 KT757840 AF416834 AF416860 SBMNH235066, USNM803530 Sheldonella bisulcata (Lamarck, 1819) MZSP26911 Striarca lactea (Linnaeus, 1758) AF120531 KT757855 AF120646 USNM857645, MCZ379156 Striarca symmetrica (Reeve, 1844) MZSP55574 Glycymerididae Glycymeris decussata (Linnaeus, 1758) MZSP91966 Glycymeris gigantea (Reeve, 1843) KT757794 KT757841 KT757883 MCZ 378989 Glycymeris glycymeris (Linnaeus, 1758) KC429328 KC429421 KC429093 KC429163 USNM794960 Glycymeris holoserica (Reeve, 1843) KT757796 KT757843 KT757885 MCZ378984 Glycymeris longior (G. B. Sowerby, 1833) MZSP91201, ZUECBIV78 Glycymeris nummaria (Linnaeus, 1758) KT757798 KT757845 KX785178 KT757887 MCZ378985 Glycymeris septentrionalis (Middendorff, 1849) KT757799 KT757846 KF643645 KT757888 Glycymeris tenuicostata (Reeve, 1843) KT757800 KT757847 KT757889 MCZ378982 Glycymeris undata (Linnaeus, 1758) MZSP91983 Tucetona pectinata (Gmelin, 1791) KT757812 KT757859 KX713507 KT757900 MZSP91971, ZUECBIV2198 Limopsidae Limopsis aurita (Brocchi, 1814) ZUECBIV2248, MCZ348438 Limopsis cristata Jeffreys, 1876 MZSP104154, MCZ348410 Limopsis cumingi Adams, 1863 KT757802 AB076930 Limopsis enderbyensis Powell, 1958 AJ422057 AY321301 Limopsis galatheae Knudsen, 1970 MCZ348437 Limopsis lilliei E. A. Smith, 1915 MZSP90647, USNM904585 Limopsis marionensis E. A. Smith, 1885 AJ422058 AY321303 USNM760835, USNM886526 Limopsis sp. Sassi, 1827 KC429329 KC429422 KC429164 Limopsis sulcata Verrill & Bush, 1898 USNM832925 Limopsis tenella Jeffreys, 1876 USNM807040 Philobryidae Adacnarca nitens Pelseneer, 1903 KP340836 KT757815 KT757862 MZSP90616, USNM886551 Lissarca notorcardensis Melvill & Standen, 1907 EF192520 KF612434 MZSP87826, USNM899485 Neocardia sp. G. B. Sowerby III, 1892 KT757804 KT757850 KX713486 KT757891 USNM881121, MCZ378927 Philobrya magellanica (Stempell, 1899) KP340845 KT757853 KT757895 Philobrya sublaevis Pelseneer, 1903 KP340835 KP340812 MZSP90645, USNM882353 Outgroup: Pteriomorphia Lima lima (Linnaeus, 1758) KC429339 KC429434 KC429101 KC429174 USNM 754383 Malleus albus Lamarck, 1819 KC429334 HQ329464 KC429097 KC429169 MZSP55595 Mytilus edulis Linnaeus, 1758 KC429331 KC429424 KF644190 KC429166 MZSP120321 Ostrea edulis Linnaeus, 1758 L49052 AF137047 AF120651 AY070151 USNM836256 Pecten maximus (Linnaeus, 1758) L49053 HM630545 KC429102 EU379508 Pinctada margaritifera (Linnaeus, 1758) AB214451 AB214466 AB259166 HQ329296 USNM836493 Pinna carnea Gmelin, 1791 HQ329375 KJ366067 KJ366325 KC429172 MZSP29040 Outgroup: Bivalvia Chione elevata (Say, 1822) KC429387 KC429495 KC429136 KC429219 Macoma balthica (Linnaeus, 1758) KC429393 KC429501 KC429141 KC429224 Margaritifera margaritifera (Linnaeus, 1758) AF229612 KC429443 AF303316 KC429185 Neotrigonia lamarckii (Gray, 1838) KC429345 KC429443 KC429105 KC429182 Nucula sulcuta Bronn, 1831 AF207642 KC984815 KC984746 KC984777 Taxa Reference 18S rRNA 28S rRNA COI mtDNA Histone H3 Collections Arcidae Acar dominguensis (Lamarck, 1819) FJ480593 KT757861 MZSP118292 Acar gradata (Broderip & Sowerby I, 1829) USNM796185 Acar plicata (Dillwyn, 1817) AJ389630 AJ307533 FJ480453 AF416856 MZSP115322 Anadara antiquata (Linnaeus, 1758) JN974491 JN974542 HQ258850 JN974592 MZSP99848 Anadara baughmani Hertlein, 1951 USNM803522 Anadara broughtonii (Schrenck, 1867) JN974489 JN974541 HQ258847 JN974590 USNM802331 Anadara chemnitzii (Philippi, 1851) MZSP43259, ZUECBIV4870 Anadara cornea (Reeve, 1844) JN974499 DQ343860 HQ258856 JN974600 Anadara crebricostata (Reeve, 1844) JN974495 JN974547 HQ258859 JN974596 Anadara ferruginea (Reeve, 1944) SBMNH81002 Anadara floridana (Conrad, 1869) USNM847847 Anadara globosa (Reeve, 1844) JN974484 JN974535 HQ258861 JN974584 Anadara grandis (Broderip & Sowerby I, 1829) USNM803487 Anadara gubernaculum (Reeve, 1844) JN974493 JN974544 HQ258857 JN974594 Anadara inaequivalvis (Bruguiere, 1789) JN974497 JN974548 AB076937 JN974598 MZSP55060 Anadara notabilis (Röding, 1798) KT757768 KT757816 AF416828 KT757863 MZSP84987, MZSP84886 Anadara obesa (G. B. Sowerby I, 1833) MCZ337676 Anadara pilula (Reeve, 1843) JN974507 JN974558 HQ258862 JN974608 Anadara subcrenata (Lischle, 1869) JN974501 DQ343861 HQ258851 JN974602 Anadara transversa (Say, 1822) USNM801135, MCZ359001 Anadara trapezia (Deshayes, 1839) KT757770 KT757817 KX713443 KT757865 SBMNH10187 Anadara vellicata (Reeve, 1844) JN974487 JN974539 HQ258848 JN974588 Arca imbricata Bruguière, 1789 AY654986 KT757820 AF253494 AY654989 MZSP95208, MZSP109869 Arca navicularis Bruguière, 1789 JN974517 KT757821 HQ258822 JN974618 USNM719071, MCZ378833 Arca noae Linnaeus, 1758 KC429325 KT757822 KC429090 KC429160 USNM1086014 Arca patriarchalis Röding, 1798 JN974527 JN974576 JN974627 MZSP99765 Arca ventricosa (Lamarck, 1819) AB076935 AF416854 MZSP55027 Arca zebra (Swainson, 1833) KT757776 KT757824 AF416864 MZSP101688 Barbatia amygdalumtostum (Röding, 1798) JN974526 JN974575 JN974626 SBMNH349329, USNM847011 Barbatia barbata (Linnaeus, 1758) KC429326 KT757825 KC429091 KC429161 MCZ378867 Barbatia cancellaria (Lamarck, 1819) KT757779 KT757827 MZSP32336, MZSP48857 Barbatia candida (Helbling, 1779) KT757784 KT757831 AF253487 AF416849 MZSP105572, ZUECBIV1407 Barbatia lacerata (Bruguière, 1789) JN974509 JN974560 HQ258826 JN974610 Barbatia lima (Reeve, 1844) JN974511 JN974563 HQ258837 JN974612 MZSP71135 Barbatia virescens (Reeve, 1844) JN974524 KT757835 HQ258840 JN974624 MZSP71367, MCZ378874 Bathyarca corpulenta (E. A. Smith, 1885) SBMNH349320 Bathyarca glomerula (Dall, 1881) KT757790 KT757837 KT757880 Bathyarca pectunculoides (Scacchi, 1835) MCZ348402 Bentharca asperula (Dall, 1881) MCZ348399 Lunarca ovalis (Bruguière, 1789) GQ166571 AF416844 MZSP84823, USNM803532 Tegillarca granosa (Linnaeus, 1758) JN974505 KT757857 HQ258867 JN974606 MZSP55596, MCZ378820 Tegillarca nodifera (Martens, 1860) JN974503 JN974554 HQ258869 JN974604 Trisidos kiyonoi (Makiyama, 1931) JN974522 JN974571 HQ258846 JN974622 SBMNH97422, SBMNH97423 Trisidos tortuosa (Linnaeus, 1758) KT757811 KT757858 KT757899 Cucullaeidae Cucullaea labiata (Lightfoot, 1786) JN974513 JN974565 KJ774477 JN974614 USNM746883 Noetiidae Arcopsis adamsi (Dall, 1886) KC429327 KC429419 KC429092 KC429162 MZSP19724, ZUECBIV1153 Didimacar tenebrica (Reeve, 1844) JN974515 JN974566 HQ258870 JN974616 SBMNH80722 Eontia ponderosa (Say, 1822) KT757793 KT757840 AF416834 AF416860 SBMNH235066, USNM803530 Sheldonella bisulcata (Lamarck, 1819) MZSP26911 Striarca lactea (Linnaeus, 1758) AF120531 KT757855 AF120646 USNM857645, MCZ379156 Striarca symmetrica (Reeve, 1844) MZSP55574 Glycymerididae Glycymeris decussata (Linnaeus, 1758) MZSP91966 Glycymeris gigantea (Reeve, 1843) KT757794 KT757841 KT757883 MCZ 378989 Glycymeris glycymeris (Linnaeus, 1758) KC429328 KC429421 KC429093 KC429163 USNM794960 Glycymeris holoserica (Reeve, 1843) KT757796 KT757843 KT757885 MCZ378984 Glycymeris longior (G. B. Sowerby, 1833) MZSP91201, ZUECBIV78 Glycymeris nummaria (Linnaeus, 1758) KT757798 KT757845 KX785178 KT757887 MCZ378985 Glycymeris septentrionalis (Middendorff, 1849) KT757799 KT757846 KF643645 KT757888 Glycymeris tenuicostata (Reeve, 1843) KT757800 KT757847 KT757889 MCZ378982 Glycymeris undata (Linnaeus, 1758) MZSP91983 Tucetona pectinata (Gmelin, 1791) KT757812 KT757859 KX713507 KT757900 MZSP91971, ZUECBIV2198 Limopsidae Limopsis aurita (Brocchi, 1814) ZUECBIV2248, MCZ348438 Limopsis cristata Jeffreys, 1876 MZSP104154, MCZ348410 Limopsis cumingi Adams, 1863 KT757802 AB076930 Limopsis enderbyensis Powell, 1958 AJ422057 AY321301 Limopsis galatheae Knudsen, 1970 MCZ348437 Limopsis lilliei E. A. Smith, 1915 MZSP90647, USNM904585 Limopsis marionensis E. A. Smith, 1885 AJ422058 AY321303 USNM760835, USNM886526 Limopsis sp. Sassi, 1827 KC429329 KC429422 KC429164 Limopsis sulcata Verrill & Bush, 1898 USNM832925 Limopsis tenella Jeffreys, 1876 USNM807040 Philobryidae Adacnarca nitens Pelseneer, 1903 KP340836 KT757815 KT757862 MZSP90616, USNM886551 Lissarca notorcardensis Melvill & Standen, 1907 EF192520 KF612434 MZSP87826, USNM899485 Neocardia sp. G. B. Sowerby III, 1892 KT757804 KT757850 KX713486 KT757891 USNM881121, MCZ378927 Philobrya magellanica (Stempell, 1899) KP340845 KT757853 KT757895 Philobrya sublaevis Pelseneer, 1903 KP340835 KP340812 MZSP90645, USNM882353 Outgroup: Pteriomorphia Lima lima (Linnaeus, 1758) KC429339 KC429434 KC429101 KC429174 USNM 754383 Malleus albus Lamarck, 1819 KC429334 HQ329464 KC429097 KC429169 MZSP55595 Mytilus edulis Linnaeus, 1758 KC429331 KC429424 KF644190 KC429166 MZSP120321 Ostrea edulis Linnaeus, 1758 L49052 AF137047 AF120651 AY070151 USNM836256 Pecten maximus (Linnaeus, 1758) L49053 HM630545 KC429102 EU379508 Pinctada margaritifera (Linnaeus, 1758) AB214451 AB214466 AB259166 HQ329296 USNM836493 Pinna carnea Gmelin, 1791 HQ329375 KJ366067 KJ366325 KC429172 MZSP29040 Outgroup: Bivalvia Chione elevata (Say, 1822) KC429387 KC429495 KC429136 KC429219 Macoma balthica (Linnaeus, 1758) KC429393 KC429501 KC429141 KC429224 Margaritifera margaritifera (Linnaeus, 1758) AF229612 KC429443 AF303316 KC429185 Neotrigonia lamarckii (Gray, 1838) KC429345 KC429443 KC429105 KC429182 Nucula sulcuta Bronn, 1831 AF207642 KC984815 KC984746 KC984777 Nucleotide sequences were obtained in the GenBank database; accession numbers are listed. Morphological investigation was conducted with taxa included in the phylogenetic study (when possible) and additional species; catalogue numbers are indicated. Abbreviations: MCZ, Museum of Comparative Zoology; MZSP, Museum of Zoology of the University of São Paulo; SBMNH, Santa Barbara Museum of Natural History; USNM, Smithsonian National Museum of Natural History; ZUECBIV, Museum of Zoology ‘Prof. Adão José Cardoso’ of the University of Campinas. View Large Morphological investigation of the mantle margin included data from 64 species obtained from preserved specimens of the following collections: Museum of Comparative Zoology (MCZ), Museum of Zoology ‘Prof. Adão José Cardoso’ of the University of Campinas (ZUECBIV), Museum of Zoology of the University of São Paulo (MZSP), Smithsonian National Museum of Natural History (USNM) and Santa Barbara Museum of Natural History (SBMNH). Respective catalogue numbers are listed in Table 1. From the 64 species studied for morphology, 38 species have available sequences used for phylogenetic inference, and 26 species either belong to genera that include the remaining sequenced species or correspond to taxa included to complement the observations (Table 1). One to five specimens per species were dissected depending on the availability of preserved material. Phylogenetic analysis and divergence times Sequence alignments were generated with MAFFT v.7.311 under the L-INS-i option (accurate strategy) (Katoh & Standley, 2013). ModelFinder (Kalyaanamoorthy et al., 2017) was used to obtain the best-fitting model of sequence evolution under the corrected Akaike information criterion (AICc), returning GTR+I+G for the concatenated dataset, which was applied in subsequent analyses. Maximum likelihood (ML) analysis was conducted in IQ-TREE (Nguyen et al., 2014), and node support was estimated by standard non-parametric bootstrap (100 replicates) (Felsenstein, 1985). Divergence times of clades were estimated by Bayesian inference (BI) in RevBayes v.1.0.9 under the fossilized birth–death model (Heath et al., 2014; Höhna et al., 2016). This model imposes a time structure on the tree by marginalizing over all possible attachment points for the fossils on the extant tree. In addition, instead of treating the calibration density as an additional prior distribution on the tree, the model treats it as the likelihood of the fossil data given the tree parameter (Heath et al., 2014). Following Bieler et al. (2014), the root age for Bivalvia was constrained, applying a uniform distribution prior between 520.5 and 530 Mya based on the fossil Fordilla troyensis (Pojeta et al., 1973). Four additional fossils were used to calibrate internal node ages, three of them previously adopted elsewhere (Combosch & Giribet, 2016). The age of Arcida was constrained around 478.6 ± 5 Mya, based on Glyptarca serrata (Cope, 1997). Glycymerididae was constrained around 167.7 ± 5 Mya, based on Trigonarca tumida (Imlay, 1962). The fossil of Anadara ferruginea was used to constrain the age of the subfamily Anadarinae around 138.3 ± 5 Mya (Huber, 2010). Finally, the age of Philobryidae was constrained around 45 ± 11 Mya based on the oldest fossil records for the family (Moore & Teichert, 1969). All priors for fossil ages were drawn from uniform distributions. An uncorrelated exponential model on molecular branch rates was assumed for the relaxed molecular clock. Posterior probabilities were sampled using the Markov chain Monte Carlo method with four independent chains running for 500 000 iterations, each one containing 534 moves (changes of values in stochastic parameters). Convergence of the posteriors were observed in Tracer v.1.6 (Rambaut et al., 2018). Fossil taxa were then pruned from trees because they were used solely to calibrate node ages, rather than to infer phylogenetic placements. Subsequently, phylogenetic trees were summarized as a maximum clade credibility tree, with a burn-in of 10% removed. A lineages-through-time plot was generated in IcyTree (https://icytree.org/). Character evolution Mantle margin evolution in Arcida was studied based on morphological data for 64 species from museum collections (Table 1). Specimens were dissected in ethanol and observed under the stereomicroscope for anatomical investigation. Characters were coded, and states were assigned to terminals based on observations of the corresponding species. In the absence of data from the literature, unobserved species had their states assigned as equivalent to closest relatives (i.e. congeneric species) obtained from collections (Supporting Information, Tables S1 and S2). Characters are related to the number and relative size of mantle folds, pigmentation, the presence and type of photoreceptor organs, and presence of the mantle nerve (Supporting Information, Table S1). Given that ethanol often shrinks/distorts tissues during preservation, mantle fold length is a character defined by the relative length of a fold in comparison to another fold, rather than the absolute length. Some multistate characters were also coded as binary (see Supporting Information, Table S1), as required by the correlation test (Pagel, 1994). Information on habits of life was compiled from the literature for all species included in the phylogenetic analysis (Supporting Information, Table S3). Modes of life include: epifaunal (above the substrate, frequently attached to the surface), semi-infaunal (partly buried in soft sediment) and infaunal (buried in soft sediment), with respective modes of byssal attachment, i.e. epibyssate, endobyssate and abyssate. Additional information was also recovered, such as the type of substrate and occurrence relative to depth, varying from shallow (< 200 m) to deep waters (> 200 m). Subsequently, lifestyles were coded (Supporting Information, Tables S1 and S2) and studied for character evolution as detailed below. Ancestral state reconstructions (ASRs) were conducted under maximum likelihood in Mesquite (Maddison & Maddison, 2018). Two possible models for trait evolution were applied, i.e. the Markov k-state one-parameter model (MK1), which assumes equal transition rates, and the asymmetrical Markov k-state two-parameter model (AsymmMK), in which transition rates can be different. In contrast to the MK1 model, the AsymmMK model allows different rates for ‘forward’ (0→1) and ‘backward’ (1→0) transitions. A likelihood ratio (LR) test was used to verify which model fitted the data better (Pagel, 1999; Maddison & Maddison, 2018). Given that the two models are nested, the LR test follows a χ2 distribution, with d.f. = 1 (because the AsymmMK model has only one additional parameter compared with the MK1 model). The reconstructions presented herein follow the statistical decision to reject the null hypothesis (MK1 model) whenever LR > 3.84 (critical value for α = 0.05, d.f. = 1). To evaluate the possible effects of branch supports and alternative topologies in the reconstruction, bootstrap trees were also investigated to inspect the consistency of the reconstructed evolutionary patterns (see Maddison & Maddison, 2018). Pagel’s correlation test was applied in Mesquite (Pagel, 1994; Maddison & Maddison, 2018) to compare the evolution of modes of life and morphological traits, such as photoreceptor organs, mantle folds and pigmentation. Although the method has some shortcomings (Maddison & Fitzjohn, 2015), it provides a helpful approach to analyse the evolution of traits statistically by incorporting phylogenetic information. Additionally, tests were conducted considering models representing evolutionary dependence among traits, i.e. when the shift of state in one character is likely to depend on the state of the second character. Searches were carried out (iterations, N = 10) with the P-value being estimated from 10 000 repeated simulations. Hypotheses of character correlations were accepted whenever a model with eight parameters (correlated hypothesis) presented a better fit (P < 0.05) than a model of evolution with four parameters (uncorrelated hypothesis) (Pagel, 1994; Maddison & Fitzjohn, 2015). RESULTS Mantle margin diversity in arcida Mantle margin in arcids may comprise four marginal extensions, named mantle folds, identified according to the position relative to the periostracal groove (Fig. 1A, B). They are named, from the outside to the inside: second outer fold, first outer fold, middle fold and inner fold (Fig. 1B). The second outer fold is a short and delicate projection in a proximal position, present in most Arcida representatives. This structure is usually unpigmented and located close to the region where the pallial muscles are attached to the valve. Although this fold is apparent in ark clams and blood cockles, such as Anadara and Tegillarca (Fig. 1L), it seems to be extremely reduced or even absent in smaller species. This is the case for some Philobryidae species (e.g. Adacnarca, Lissarca and Neocardia), in which the second outer fold was not observed. The first outer fold is usually well developed in most species, frequently being pigmented and bearing photoreceptor organs. Strong pigmentation is common in epifaunal species, such as Arca (Fig. 1D), although pigmentation is also present in some semi-infaunal (e.g. Glycymerididae; Fig. 2E, F) and infaunal species (e.g. some Anadara spp.). Photoreceptor organs vary from small eyespots to large compound eyes (Figs 1, 2). Pigmented eyespots are present in epifaunal Noetiidae, such as Arcopsis (Fig. 2B), Didimacar and Stryarca, most Arcidae taxa (Fig. 1H), except Trisidos (infaunal) and Bathyarca (infaunal; deep sea), and some Philobryidae, including Lissarca notorcardensis and Neocardia sp. (Fig. 2K). These eyespots are frequently restricted to the anterodorsal region. Compound eyes are larger, multifaceted structures, occurring on the posterior region of Acar, Arca, Cucullaea (Fig. 1C, D, F), Glycymerididae (Fig. 2E, F) and some Barbatia species (Fig. 1E, G). Figure 2. View largeDownload slide Mantle margin morphology in Noetiidae (A–D), Glycymerididae (E, F), Limopsidae (G–I) and Philobryidae (J–M). Posterior mantle region. Scale bars: 1 mm. The first outer fold can bear compound eyes (arrows) and pigmented eyespots (arrowheads). A, Striarca lactea (USNM 857645). B, Arcopsis solida (USNM 733218). C, Didimacar tenebrica (SBMNH 80722). D, Noetia ponderosa (USNM 803530). E, Tucetona pectinata (MZSP 91971). F, Glycymeris tenuicostata (378982). G, Limopsis aurita (ZUEC-BIV 2248). H, Limopsis lilliei (MZSP 90647). I, Limopsis marionensis (USNM 760835). J, Adacnarca nitens (USNM 886551). K, Lissarca notorcadensis (MZSP 87826). L, Neocardia sp. (MCZ 378927). M, Philobrya sublaevis (MZSP 90645). Abbreviations: if, inner fold; ma, mantle; mm, mantle margin; of-1, first outer fold. Figure 2. View largeDownload slide Mantle margin morphology in Noetiidae (A–D), Glycymerididae (E, F), Limopsidae (G–I) and Philobryidae (J–M). Posterior mantle region. Scale bars: 1 mm. The first outer fold can bear compound eyes (arrows) and pigmented eyespots (arrowheads). A, Striarca lactea (USNM 857645). B, Arcopsis solida (USNM 733218). C, Didimacar tenebrica (SBMNH 80722). D, Noetia ponderosa (USNM 803530). E, Tucetona pectinata (MZSP 91971). F, Glycymeris tenuicostata (378982). G, Limopsis aurita (ZUEC-BIV 2248). H, Limopsis lilliei (MZSP 90647). I, Limopsis marionensis (USNM 760835). J, Adacnarca nitens (USNM 886551). K, Lissarca notorcadensis (MZSP 87826). L, Neocardia sp. (MCZ 378927). M, Philobrya sublaevis (MZSP 90645). Abbreviations: if, inner fold; ma, mantle; mm, mantle margin; of-1, first outer fold. The middle mantle fold, when present, represents a reduced projection, shorter than the first outer fold (Fig. 1E). No photoreceptor or tentacular structures are associated with this projection. The middle fold is absent in the genera Arca, Cucullaea and Trisidos (Fig. 1C, D, F, N). The mantle margin also lacks a middle fold in Glycymerididae, Philobryidae and infaunal Noetiidae (e.g. Eontia and Noetia; Fig. 2). The inner mantle fold is an enlarged, muscular projection in most arcid taxa, usually longer and robust posteriorly. In the Cucullaeidae, Glycymerididae, Limopsidae, Philobryidae and the genus Arca, the inner mantle fold is about the length of the first outer fold or slightly longer (Figs 1D, 2G–M). In contrast, the inner fold is about twice the length of the first outer fold in Noetiidae, Barbatia and Acar (Fig. 1E, G). A massive enlargement of the inner fold is observed in some Barbatia species and in numerous infaunal species, such as Trisidos, Anadara, Tegillarca, Eontia and Noetia (Fig. 1I–N). A posterior flap, formed by the inner fold, is a long projection found in Bathyarca species (Fig. 1M). The mantle margin in arcids exhibits different levels of variation among taxa. For example, the number of folds and relative lengths are very uniform within the Anadarinae (Fig. 1J–L), but highly variable within Barbatia (Fig. 1E, G–I). Within Noetiidae, mantle organization is also variable (Fig. 2A–D), whereas in Glycymerididae it is more uniform (Fig. 2E, F). In contrast, the Limopsidae (Fig. 2G–I) and Philobryidae (Fig. 2J–M) have a less complex and miniaturized mantle margin, usually devoid of photoreceptor organs, pigmentation or enlarged folds. Phylogenetic hypotheses The maximum likelihood tree of the Arcida corroborates the monophyly of the clade and the monophyly of all families, except for Arcidae, which is split into five branches (Fig. 3). Although some internal nodes show low bootstrap values, higher support was obtained for some relationships among families and genera (e.g. Arca, Anadarinae, Glycymerididae and Limopsidae). The remaining Pteriomorphia were recovered as the sister group of Arcida. Figure 3. View largeDownload slide Phylogenetic relationships within Arcida based on maximum likelihood analysis of four genes (18S rRNA, 28S rRNA, COI mtDNA and H3). Asterisks on nodes indicate bootstrap values > 95%. Selected clades are indicated by colour groups. Arcidae is the only non-monophyletic family. Figure 3. View largeDownload slide Phylogenetic relationships within Arcida based on maximum likelihood analysis of four genes (18S rRNA, 28S rRNA, COI mtDNA and H3). Asterisks on nodes indicate bootstrap values > 95%. Selected clades are indicated by colour groups. Arcidae is the only non-monophyletic family. Arcidae is polyphyletic in our analysis, with Arca and Acar descending from an early branch of the order. All Anadarinae species are nested together, being sister group to a pair of Barbatia species (Barbatia candida and Barbatia lacerata). Interestingly, Barbatia species are scattered across the phylogeny, suggesting separate lineages taxonomically included under the same name. Noetiidae is a monophyletic family, although Adacnarca nitens, formally a philobryid, seems also to be included in this clade. A close relationship between Limopsidae and Philobryidae was recovered, with Glycymerididae as the sister group. The three former families were recovered as the sister group of (Cucullaea + Bathyarca). A similar topology was recovered for the time-calibrated phylogeny (Fig. 4). Diversification times were estimated for the major lineages with the 95% highest posterior density interval (HPD): Arcida, 341.3 Mya (95% HPD 261.2–424.1 Mya); Glycymerididae, 194.6 Mya (95% HPD 112.1–278.3 Mya); Anadarinae, 190.5 Mya (95% HPD 124–256.7 Mya); Limopsoidea, 187.7 Mya (95% HPD 113.4–259.3 Mya); Noetiidae, 175.5 Mya (95% HPD 96.6–248.1 Mya); Philobryidae, 143 Mya (95% HPD 77.1–215.9 Mya); and Limopsidae, 110.4 Mya (95% HPD 37.8–195.1 Mya). A lineage-through-time plot also shows a major diversification of Arcida lineages during the Mesozoic (Fig. 4). Figure 4. View largeDownload slide Time-calibrated phylogeny of Arcida under Bayesian inference based on four genes (18S rRNA, 28S rRNA, COI mtDNA and H3) and five fossils used to calibrate internal nodes (red circles). Green values indicate median ages on selected nodes. Grey bars indicate 95% highest posterior density intervals (HPD) for nodes of interest. Posterior probabilities different from 1.0 are indicated on nodes. Colour code for clades and taxa is the same as the one used in Figure 3. A lineages-through-time plot is shown at the upper left. After a Cambrian divergence, the crown group of Arcida had an origin ~341 Mya (Carboniferous) and a major diversification during the Mesozoic. Figure 4. View largeDownload slide Time-calibrated phylogeny of Arcida under Bayesian inference based on four genes (18S rRNA, 28S rRNA, COI mtDNA and H3) and five fossils used to calibrate internal nodes (red circles). Green values indicate median ages on selected nodes. Grey bars indicate 95% highest posterior density intervals (HPD) for nodes of interest. Posterior probabilities different from 1.0 are indicated on nodes. Colour code for clades and taxa is the same as the one used in Figure 3. A lineages-through-time plot is shown at the upper left. After a Cambrian divergence, the crown group of Arcida had an origin ~341 Mya (Carboniferous) and a major diversification during the Mesozoic. Mantle margin evolution The history of changes in the mantle margin was reconstructed based on key traits. A second outer fold has arisen in the origin of the Arcida clade, and probably lost in Limopsidae and Philobryidae lineages (data not shown). Intense mantle pigmentation was acquired multiple times, i.e. in the origin of Glycymerididae, Arca + Acar, Barbatia barbata + Barbatia cancellaria + Barbatia fusca, and some lineages within Anadarinae (Supporting Information, Fig. S1). The ancestor of Arcida had a reduced middle fold, i.e. shorter than the first outer fold (Fig. 5), which is a striking contrast to the remaining Pteriomorphia, in which the middle fold is long and usually bears tentacles and photoreceptor organs. Although most arcids share a reduced middle fold, the complete loss of this projection occurred at least ten times (Fig. 5). Photoreceptor organs were reconstructed to be present in the mantle margin of the Arcida’s ancestor. More specifically, the presence of pigmented eyespots represents a plesiomorphy for all arcid taxa, with secondary losses for many infaunal lineages, such as Eontia, Limopsis and Trisidos (Fig. 6A). Likewise, compound eyes were probably present in the Arcida’s ancestor, which were subsequently lost in four separate lineages: Limopsoidea, Bathyarca, Anadarinae + (B. candida + B. lacerata), and a clade formed by Noetiidae with some Barbatia and Trisidos species (Supporting Information, Fig. S2). Figure 5. View largeDownload slide Ancestral state reconstruction of the middle mantle fold in Arcida under maximum likelihood, assuming a single rate for all possible transitions (MK1 model). Pie charts represent the likelihood proportions of reconstructed states; nodes of interest have their charts enlarged. Mantle margin schemes indicate mantle morphology as reconstructed by the analysis. Abbreviations: ce, compound eyes; if, inner fold; ma, mantle; mf, middle fold; of, outer fold; of-1, first outer fold; of-2, second outer fold; pc, pigmented eyespots; sh, shell. Figure 5. View largeDownload slide Ancestral state reconstruction of the middle mantle fold in Arcida under maximum likelihood, assuming a single rate for all possible transitions (MK1 model). Pie charts represent the likelihood proportions of reconstructed states; nodes of interest have their charts enlarged. Mantle margin schemes indicate mantle morphology as reconstructed by the analysis. Abbreviations: ce, compound eyes; if, inner fold; ma, mantle; mf, middle fold; of, outer fold; of-1, first outer fold; of-2, second outer fold; pc, pigmented eyespots; sh, shell. Figure 6. View largeDownload slide Ancestral state reconstruction of mantle photoreceptor organs (left; AsymmMK model) and mode of life (right; MK1 model) in Arcida under maximum likelihood. Ingroup is indicated by the grey boxes. Pie charts represent the likelihood proportions of reconstructed states; nodes of interest have their charts enlarged. The ancestor of Arcida is recovered as an epifaunal animal with simple eyespots on the mantle. Most subsequent losses of eyespots (red arrows on the left) are apparently associated with transitions to semi-infaunal/infaunal habits (red arrows on the right). Abbreviations: if, inner fold; ma, mantle; mf, middle fold; of, outer fold; of-1, first outer fold; pc, pigmented eyespots; sh, shell. Figure 6. View largeDownload slide Ancestral state reconstruction of mantle photoreceptor organs (left; AsymmMK model) and mode of life (right; MK1 model) in Arcida under maximum likelihood. Ingroup is indicated by the grey boxes. Pie charts represent the likelihood proportions of reconstructed states; nodes of interest have their charts enlarged. The ancestor of Arcida is recovered as an epifaunal animal with simple eyespots on the mantle. Most subsequent losses of eyespots (red arrows on the left) are apparently associated with transitions to semi-infaunal/infaunal habits (red arrows on the right). Abbreviations: if, inner fold; ma, mantle; mf, middle fold; of, outer fold; of-1, first outer fold; pc, pigmented eyespots; sh, shell. The inner fold is commonly longer than the other mantle folds in most bivalves, but in Arcida this trait displays significant variation. The inner fold is reconstructed to be about the length of the first outer fold, or only slightly longer, in the origin of the Order (Fig. 7A). The enlargement of this fold, forming a long projection about twice the length of the first outer fold, occurred in the Acar’s ancestor and in the ancestor of a large clade including Noetiidae, Anadarinae and Barbatia species (Fig. 7A). Another change in state is represented by a very enlarged inner fold, much longer than first outer fold, forming extensible curtains and flaps. This transition occurred in different clades, e.g. Trisidos, Eontia, Bathyarca and Anadarinae + Barbatia, most of them including infaunal bivalves (Fig. 7B). Figure 7. View largeDownload slide Ancestral state reconstruction of inner fold length (left) and mode of life (right) in Arcida under maximum likelihood, assuming a single rate for all possible transitions (MK1 model). Ingroup is indicated by the grey boxes. Pie charts represent the likelihood proportions of reconstructed states; nodes of interest have their charts enlarged. The inner mantle fold becomes much longer than the others in numerous lineages (red arrows on the left), which is apparently associated with transitions to semi-infaunal/infaunal habits (red arrows on the right). Abbreviations: if, inner fold; ma, mantle; of-1, first outer fold; of-2, second outer fold; sh, shell. Figure 7. View largeDownload slide Ancestral state reconstruction of inner fold length (left) and mode of life (right) in Arcida under maximum likelihood, assuming a single rate for all possible transitions (MK1 model). Ingroup is indicated by the grey boxes. Pie charts represent the likelihood proportions of reconstructed states; nodes of interest have their charts enlarged. The inner mantle fold becomes much longer than the others in numerous lineages (red arrows on the left), which is apparently associated with transitions to semi-infaunal/infaunal habits (red arrows on the right). Abbreviations: if, inner fold; ma, mantle; of-1, first outer fold; of-2, second outer fold; sh, shell. Association between mantle margin morphology and lifestyles The reconstruction of modes of life suggests that the ancestor of Arcida was likely to be an epifaunal bivalve, possibly attached to rocks and hard substrate by a byssus (Fig. 6B; Supporting Information, Table S3). Soft sediments, such as mud and sand, were later occupied independently by different groups. The semi-infaunal/infaunal lifestyle was secondarily adopted four times during Arcida evolution during the Mesozoic (Figs 4, 6B), by lineages originating Anadarinae, Trisidos, Eontia (infaunal noetiids) and the ancestor of all Limopsoidea + Glycymerididae + (Bathyarca + Cucullaeidae). Among infaunal lineages, a shift to epifaunal lifestyle has occurred in the origin of Philobryidae (Fig. 6B), animals that are frequently byssate on other organisms, such as algae. Correlation tests were applied when mantle traits seemed to be associated with particular lifestyles. For instance, pigmentation on the first outer fold is common in epifaunal bivalves. The tested hypotheses of evolutionary correlation are shown in Table 2. Pigmentation, which is typical for epifaunal bivalves, was not statistically correlated with lifestyle (Table 2). Pigmented eyespots, however, had a statistically significant correlation with lifestyle (Table 2). Ancestral state reconstructions of eyespots and lifestyles suggested that this correlation was associated with the adoption of infaunal habits and loss of pigmented eyespots (Fig. 6). Inner fold enlargement was also correlated with mode of life, with the results suggesting that the evolutionary shift to infaunal habit was more likely when the inner fold became much longer than the first outer fold (Table 2). Table 2. Evolutionary correlation tests between mantle margin traits and lifestyles in Arcida Morphological traits (y) and hypotheses (h) Mode of life: epifaunal vs. infaunal (x) Difference in −logL between models P-value Conclusion First outer fold pigmentation  h1 correlation 2.8321 0.138 Independent traits Compound eyes  h1 correlation 0.9473 0.268 Independent traits Pigmented eyespots  h1 correlation 5.12 0.0223 Correlated traits  h2x depends on y 0.4789 0.3884 x does not depend on y  h3y depends on x 2.0402 0.13 y does not depend on x Inner mantle fold development  h1 correlation 6.4797 0.002 Correlated traits  h2x depends on y 2.3043 0.0112 x depends on y  h3y depends on x 3.1362 0.0569 y does not depend on x Morphological traits (y) and hypotheses (h) Mode of life: epifaunal vs. infaunal (x) Difference in −logL between models P-value Conclusion First outer fold pigmentation  h1 correlation 2.8321 0.138 Independent traits Compound eyes  h1 correlation 0.9473 0.268 Independent traits Pigmented eyespots  h1 correlation 5.12 0.0223 Correlated traits  h2x depends on y 0.4789 0.3884 x does not depend on y  h3y depends on x 2.0402 0.13 y does not depend on x Inner mantle fold development  h1 correlation 6.4797 0.002 Correlated traits  h2x depends on y 2.3043 0.0112 x depends on y  h3y depends on x 3.1362 0.0569 y does not depend on x The test compares the four-parameter model (independent evolution; h0) and the eight-parameter models (correlated evolution; h1, h2 and h3) between two binary traits, returning the differences in log-likelihood (−logL) with P-values calculated by 10 000 simulations. Significant differences, i.e. P-value < α = 0.05, indicate a better fit to the model of correlated evolution. Characters and respective states: first outer fold pigmentation, absent (0) or present (1); compound eyes, absent (0) or present (1); pigmented eyespots, absent (0) or present (1); inner mantle fold development, up to twice the length (0) or much longer (1) than the first outer fold; mode of life, epifaunal (0) or semi-infaunal/infaunal (1). View Large Table 2. Evolutionary correlation tests between mantle margin traits and lifestyles in Arcida Morphological traits (y) and hypotheses (h) Mode of life: epifaunal vs. infaunal (x) Difference in −logL between models P-value Conclusion First outer fold pigmentation  h1 correlation 2.8321 0.138 Independent traits Compound eyes  h1 correlation 0.9473 0.268 Independent traits Pigmented eyespots  h1 correlation 5.12 0.0223 Correlated traits  h2x depends on y 0.4789 0.3884 x does not depend on y  h3y depends on x 2.0402 0.13 y does not depend on x Inner mantle fold development  h1 correlation 6.4797 0.002 Correlated traits  h2x depends on y 2.3043 0.0112 x depends on y  h3y depends on x 3.1362 0.0569 y does not depend on x Morphological traits (y) and hypotheses (h) Mode of life: epifaunal vs. infaunal (x) Difference in −logL between models P-value Conclusion First outer fold pigmentation  h1 correlation 2.8321 0.138 Independent traits Compound eyes  h1 correlation 0.9473 0.268 Independent traits Pigmented eyespots  h1 correlation 5.12 0.0223 Correlated traits  h2x depends on y 0.4789 0.3884 x does not depend on y  h3y depends on x 2.0402 0.13 y does not depend on x Inner mantle fold development  h1 correlation 6.4797 0.002 Correlated traits  h2x depends on y 2.3043 0.0112 x depends on y  h3y depends on x 3.1362 0.0569 y does not depend on x The test compares the four-parameter model (independent evolution; h0) and the eight-parameter models (correlated evolution; h1, h2 and h3) between two binary traits, returning the differences in log-likelihood (−logL) with P-values calculated by 10 000 simulations. Significant differences, i.e. P-value < α = 0.05, indicate a better fit to the model of correlated evolution. Characters and respective states: first outer fold pigmentation, absent (0) or present (1); compound eyes, absent (0) or present (1); pigmented eyespots, absent (0) or present (1); inner mantle fold development, up to twice the length (0) or much longer (1) than the first outer fold; mode of life, epifaunal (0) or semi-infaunal/infaunal (1). View Large DISCUSSION Phylogenetic relationships and divergence times Arcida is a well-supported, monophyletic group (see also Bieler et al., 2014; Feng et al., 2015; Combosch & Giribet, 2016). All families were recovered as monophyletic, with the exceptions of a polyphyletic Arcidae and the placement of the philobryid Adacnarca nitens within Noetiidae. Although a previous analysis found support to separate Arcoidea from Limopsoidea (Combosch & Giribet, 2016), our results indicate Arcoidea as non-monophyletic. This is the consequence of an early branch giving rise to Acar and Arca, whereas Limopsoidea is nested within the remaining Arcoidea. Therefore, the Limopsoidea would have an origin from within the Arcoidea, a hypothesis not supported by previous topologies (Combosch & Giribet, 2016), but already suggested elsewhere (Jackson et al., 2015). Our topology is consistent with the view that Limopsidae and Philobryidae share an exclusive, common history based on similar development of hinge and alivincular ligament type (Malchus & Warén, 2005; Oliver & Holmes, 2006). The taxonomic position of Glycymerididae has always been controversial, and our data support this family within Arcoidea, as also suggested by Combosch & Giribet (2016). In contrast to their results, however, the Glycymerididae is the sister group of Limopsoidea in our analysis, forming a clade closely related to Cucullaea and Bathyarca. The Glycymerididae was previously thought to have originated from the Cucullaeidae based on the duplivincular ligament and other shell characters observed in fossil species (Nicol, 1950). Our results do not corroborate this view, but their morphological similarity is supported by the close relationship between these families. Arcidae is not monophyletic in our analyses, which is consistent with previous studies (Marko, 2002; Matsumoto, 2003; Feng et al., 2015; Combosch & Giribet, 2016). For instance, the genus Barbatia is polyphyletic, and thus in great need of taxonomic revisions. Similar to previous findings (Combosch & Giribet, 2016), some Barbatia species, such as B. candida and B. lacerata, form the sister group of Anadarinae, whereas others, such as Barbatia virescens, are close to Trisidos and Noetiidae. The oldest fossils of Arcida, i.e. Glyptarca serrata, date back to the Ordovician (~480 Mya; Cope, 1997). According to our analysis, the arcid divergence occurred in the late Cambrian (~488 Mya), and the crown group of Arcida had a Carboniferous origin, ~341 Mya. Our time-calibrated phylogeny agrees with the fossil record (Thomas, 1978a; Oliver & Holmes, 2006), suggesting that most diversification of Arcida occurred during the Mesozoic, including the origin of most modern families, i.e. Cucullaeidae, Glycymerididae, Limopsidae and Philobryidae. The convergent transitions to semi-infaunal or infaunal habits by different lineages, such as noetiids, Anadarinae, Cucullaeidae, Glycymerididae and Limopsidae, may have contributed to the diversification of Arcida, which is consistent with the Cretaceous fossil record (Thomas, 1978b; Thomas et al., 2000; Oliver & Holmes, 2006; Combosch & Giribet, 2016). The adoption of an infaunal lifestyle in bivalves is regarded as one of the most important strategies to avoid predation by a diversity of duraphagous predators during the long-lasting ecological arms race of the so-called Mesozoic marine revolution (Stanley, 1968; Vermeij, 1977). Our results, therefore, provide further evidence for the Mesozoic infaunalization of bivalves. Evolution of mantle traits and lifestyle The second outer mantle fold is an exclusive feature of Arcida, shared by most of its descendants (see also Waller, 1980). Photoreceptor organs on the first outer fold are also distinctive traits of Arcida, and they are present mainly in epifaunal species inhabiting shallow waters (Waller, 1980; Morton & Peharda, 2008; Morton & Puljas, 2015; Audino & Marian, 2018; present study). Our data support the correlated evolution of photoreceptor organs and mode of life, as previously suggested based on morphological studies alone (Audino & Marian, 2018). The Arcida’s ancestor had pigmented eyespots and posterior compound eyes that were lost in numerous lineages (Fig. 6; Supporting Information, Fig. S2). These findings suggest an important role of light-guided behaviours in ancestral ark clams living on the substrate, possibly related to predator detection and posture control (Nilsson, 1994). A single origin of compound eyes is in accordance with the anatomical similarity of these organs in the distinct arcidan lineages that have been studied so far, such as Glycymerididae, the genera Arca and Acar, and some Barbatia species (Waller, 1980; Morton & Puljas, 2015; Audino & Marian, 2018). Additionally, the loss of photoreceptor organs also provides important insights into the evolution of ark clams. Infaunal lineages frequently lost photoreceptor organs present in their epifaunal ancestor (Fig. 6; Supporting Information, Fig. S2), which can be explained either by a condition of relaxed selection under the infaunal condition or a positive selective pressure for eye reduction. Relaxed selection can be defined as the elimination or reduction, by means of environmental changes, of a selective force that was important for the maintenance of a particular trait (Lahti et al., 2009). This is an evolutionary process frequently evoked to explain eye and pigment reduction in several groups, including numerous lineages of cave animals (Porter & Crandall, 2003; Wilkens, 2010). Alternatively, other processes can also produce similar patterns. For example, variability in eye size and pigmentation in cave fishes occurs through multiple mechanisms, suggesting different evolutionary forces synergistically driving eye regression via pleiotropy (Protas et al., 2008). Studies of both vertebrate and invertebrate cave lineages have also demonstrated the high energetic costs of maintaining sensory systems, such as eyes, even in dark conditions (Niven & Laughlin, 2008). For example, eye loss in cavefishes may have been driven by selection for regression of neural tissue, which is associated with high metabolic costs (Moran et al., 2015). In cave crabs, eye reduction seems most likely to be driven by strong directional selective regimes in the subterranean environment (Klaus et al., 2013). In the marine infaunal context, our results provide the initial steps to understand the evolutionary trajectory of photoreceptor organs in ark clams. Similar to many intriguing cases of cave lineages (Niven and Laughlin, 2008), further studies are still necessary to clarify whether eye loss in infaunal bivalves is produced by selective pressure or by genetic drift when selective pressures for eye maintenance are absent. The middle fold is a mantle margin projection that is well developed in most bivalves, frequently bearing associated structures and playing sensorial roles (Yonge, 1983). An opposite condition was observed in most specimens studied herein, in which the middle fold was shorter than the outer and inner folds, corresponding to only a slight projection, when present. A shorter middle fold was also noted in Limopsis cristata (Morton, 2013) and Barbatia species (Simone & Chichvarkhin, 2004). Our results suggest that this fold was already reduced in the ancestor of Arcida, which is a remarkable difference from other pteriomorphians, which frequently display a long and complex projection (Audino & Marian, 2016). The reduction of the middle fold seems to have been a common phenomenon during Arcida diversification, resulting in the complete loss of this structure in several lineages (Fig. 5). This evolutionary pattern is unique among bivalves and leaves many unsolved functional questions. One possible explanation was provided by Morton (1982), who suggested that sensorial roles, such as photoreception, were transferred to the first outer fold. In addition, recent anatomical evidence from different arcid species also corroborated this view, indicating that chemo-/mechanosensorial roles were possibly transferred to the enlarged inner fold (Audino & Marian, 2018). The hypertrophy of the inner fold in a very extensible organ is observed in many lineages of Arcida (Fig. 7). For example, most semi-infaunal or infaunal arcids, such as some Noetiidae, Anadarinae, Trisidos and Bathyarca, have very long inner folds (see also Morton, 1982; Audino & Marian, 2018). In infaunal bivalves of other clades (e.g. Heterodonta), siphons (i.e. long, fused inner folds) are present and allow them to inhabit soft sediments and maintain water circulation through the pallial cavity (Yonge, 1983). In the case of the infaunal Bathyarca pectunculoides, the posterior flaps formed by the inner fold are thought to act as functional siphons (Morton, 1982). Accordingly, our phylogenetic and morphological data strongly support the evolution of the inner fold as a functional siphon in arcid lineages, which has possibly facilitated the transition to infaunal lifestyles. Evolutionary convergence and macroevolution Ecological shifts shaping morphological evolution are known for many vertebrate groups [e.g. lizards (Mahler et al., 2013), fishes (Davis & Betancur-R, 2017) and snakes (Esquerré & Scott Keogh, 2016)]. Although marine invertebrates still lack detailed information about ecomorphological evolution, recent progress has been achieved using different clades as models. In cephalopods, for example, several morphological traits represent evolutionary convergences and possible adaptive features associated with benthic or pelagic environments (Lindgren et al., 2012). Although bivalves have traditionally been considered classic examples of convergent evolution associated with lifestyles in the marine benthos (e.g. Stanley, 1972), even in invertebrate zoology textbooks (e.g. Ruppert et al., 2004), these adaptive hypotheses have rarely been tested under an explicit phylogenetic approach. In this context, important progress was recently obtained for Pectinidae (Alejandrino et al., 2011; Serb et al., 2017) and Galeommatoidea (Li et al., 2016). The Arcida have been consistently regarded as an example of adaptive radiation, with their homoplastic shell characters adapted to infaunal and epifaunal modes of life (Stanley, 1968, 1972; Thomas, 1976, 1978a). Our study provides, for the first time, phylogenetic-based evidence for correlated evolution between the morphology of soft parts and lifestyle transitions in arcids. In addition, evolutionary convergence seems to be a recurrent pattern, including independent losses of eyespots, compound eyes, pigmentation and the middle fold, in addition to independent enlargements of the inner fold. Our results suggest that predation pressure was important in the evolution of Arcida, mainly during the Mesozoic. Pigmented eyespots and compound eyes may aid in predator recognition in epifaunal bivalves (Nilsson, 1994), and the infaunal habit itself, facilitated by enlarged mantle curtains, might have been a response to predation pressure (Bush & Bambach, 2011). The dramatic increase of infaunal lineages in the marine benthos suggests a successful trend to survive the intensification of predation during the Mesozoic marine revolution (Stanley, 1968, 1972; Vermeij, 1977). In addition to the extensive fossil information for hard parts, we were able to contribute to this hypothesis based on the soft parts of extant lineages of arcids in an integrative approach. Altogether, our results demonstrate evolutionary associations between ecology and morphology during the diversification of bivalve lineages across different benthic lifestyles. SUPPORTING INFORMATION Additional Supporting Information may be found in the online version of this article at the publisher's web-site: Table S1. Characters and states used to study mantle margin traits and lifestyles in Arcida. Table S2. Matrix of mantle margin traits and taxa used in the analyses. Table S3. Lifestyle compilation of ark clams and relatives (Arcida) according to mode of attachment on the substrate and position. Figure S1. Ancestral state reconstruction of pigmentation on the first outer mantle fold in Arcida under maximum likelihood, assuming a single rate for all possible transitions (MK1 model). Pie charts represent the likelihood proportions of reconstructed states. Pigmentation has evolved multiple times in different lineages of epifaunal and infaunal arcids. Figure S2. Ancestral state reconstruction of compound eyes on the first outer mantle fold in Arcida under maximum likelihood, allowing for a different rate for transitions (AsymmMK model). Pie charts represent the likelihood proportions of reconstructed states. Compound eyes have a single origin in the ancestor of Arcida, with subsequent losses in at least four lineages. Abbreviations: ce, compound eyes; if, inner fold; ma, mantle; mf, middle fold; of-1, first outer fold; of-2, second outer fold; sh, shell. ACKNOWLEDGEMENTS The authors acknowledge the grants 2015/09519-4 and 2017/01365-3 from the São Paulo Research Foundation (FAPESP). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES), finance code 001. This study is part of J.A.A.’s PhD thesis through the Graduate Program in Zoology of the Institute of Biosciences (University of São Paulo). 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TI - Ark clams and relatives (Bivalvia: Arcida) show convergent morphological evolution associated with lifestyle transitions in the marine benthos
JF - Biological Journal of the Linnean Society
DO - 10.1093/biolinnean/blz017
DA - 2019-03-27
UR - https://www.deepdyve.com/lp/oxford-university-press/ark-clams-and-relatives-bivalvia-arcida-show-convergent-morphological-hkz3BLXVRJ
SP - 866
VL - 126
IS - 4
DP - DeepDyve
ER -