Fossil-Calibrated Molecular Phylogeny of Atlantid Heteropods 2 (Gastropoda, Pterotracheoidea) 3 4 Deborah Wall-Palmer1, * 5 Arie W
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1 Fossil-calibrated molecular phylogeny of atlantid heteropods 2 (Gastropoda, Pterotracheoidea) 3 4 Deborah Wall-Palmer1, * 5 Arie W. Janssen 1 6 Erica Goetze 2 7 Le Qin Choo 1, 3 8 Lisette Mekkes 1, 3 9 Katja T.C.A. Peijnenburg 1, 3 10 11 1 Marine Biodiversity Group, Naturalis Biodiversity Center, Leiden, The Netherlands. 12 13 2 Department of Oceanography, University of Hawai’i at Mānoa, Honolulu, USA. 14 15 3 Institute for Biodiversity and Ecosystem Dynamics (IBED), University of Amsterdam, 16 Amsterdam, The Netherlands. 17 18 * Corresponding author 19 Email: [email protected] 20 21 1 22 Abstract 23 24 The aragonite shelled, planktonic gastropod family Atlantidae (shelled heteropods) is 25 likely to be one of the first groups to be impacted by imminent ocean changes, 26 including ocean warming and ocean acidification. With a fossil record spanning at 27 least 100 Million years (Ma), atlantids have experienced and survived global-scale 28 ocean changes and extinction events in the past. However, the diversification 29 patterns and tempo of evolution in this family are largely unknown. Based on a 30 concatenated maximum likelihood phylogeny of three genes (cytochrome c oxidase 31 subunit 1 mitochondrial DNA, 28S and 18S ribosomal rRNA) we show that the three 32 extant genera of the family Atlantidae, Atlanta, Protatlanta and Oxygyrus, form 33 monophyletic clades. The genus Atlanta is split into two groups, one exhibiting 34 smaller, well ornamented shells, and the other having larger, less ornamented shells. 35 The fossil record, in combination with a fossil-calibrated phylogeny suggest that large 36 scale atlantid extinction was accompanied by considerable and rapid diversification 37 over the last 25 Ma, potentially driven by vicariance events. Now confronted with a 38 rapidly changing modern ocean, the ability of atlantids to survive past global change 39 crises gives some optimism that they may be able to persist through the 40 Anthropocene. 41 42 [195 of 350 words] 43 44 Keywords 45 46 Atlantidae, Planktonic gastropods, cytochrome c oxidase subunit 1, 28S and 18S 47 ribosomal rRNA, ocean change, rapid diversification 48 49 [6 of 10 keywords] 2 50 Introduction 51 52 The Atlantidae is a family of small (<14 mm) marine predatory gastropods with a 53 holoplanktonic mode of life (Fig. 1). Atlantids fall within the superfamily 54 Pterotracheoidea, known commonly as heteropods, or sea elephants. Unlike the 55 other two heteropod families (Carinariidae and Pterotracheidae), all three genera of 56 the Atlantidae (Atlanta, Protatlanta and Oxygyrus) have thin-walled laterally 57 compressed aragonite shells that are broadened with a keel. A modified foot serves 58 as a primary swimming fin, and the broad shell is used as a secondary swimming fin 59 [1]. Together, the fin and the shell generate rapid and directed movement for prey 60 capture and predator evasion. Atlantids are able to fully withdraw into their shell and 61 seal the aperture with an operculum. They also have well developed eyes, a sucker 62 on their fin for securing prey, and a proboscis, or trunk, which is used for reaching 63 into the shells of prey, such as shelled pteropods [2–4]. It is clear that atlantids have 64 remarkable and derived adaptations for a holoplanktonic lifestyle, however, their 65 evolutionary history is largely unknown. Until now, theories about the evolution of 66 atlantids (and heteropods in general) have relied upon a fossil record with vast gaps 67 [5], due to a combination of the loss of delicate aragonite shells during diagenetic 68 processes, creating genuine gaps in the fossil record, and a lack of research on fossil 69 heteropods as a whole, creating knowledge gaps. Despite these gaps, the 70 evolutionary history of this group is of interest in understanding how these delicate 71 aragonite-shelled plankton, and presently the only aragonite shelled predatory 72 holoplankton, have fared through past climate change and ocean acidification events. 73 The morphologically similar aragonite-shelled pteropods are known to have survived 74 through both the Cretaceous-Paleogene (KPg or KT) extinction event and the 75 Paleocene Eocene Thermal Maximum (PETM), which were both times of extreme 76 climate change and the closest analogues to predicted ocean changes [6–8]. 77 78 The thin-walled aragonite shells of the atlantids, and their habitat in the upper ocean 79 imply that they are likely to be sensitive to ocean acidification and ocean warming, in 80 a similar way to the shelled pteropods [9]. The only study addressing the effects of 81 ocean acidification on atlantids found negative effects of reduced ocean pH on shell 82 growth and the down-regulation of biomineralisation and growth genes [10]. 83 Relatively recent local extinctions have been reported for several atlantid species. 84 Atlanta plana and Atlanta turriculata are not found in the modern Atlantic Ocean [11], 3 85 however, fossils of both species have been found in Late Pleistocene sediments of 86 the Caribbean Sea [12], and A. plana has also been found in Pliocene rocks of 87 southern France and southern Spain [13, 14]. These records suggest the local 88 extinction of A. turriculata at around 16 thousand years (ka), and A. plana in the last 89 3.5–1 ka. Protatlanta sculpta is currently only known from the Atlantic Ocean, but 90 was present in Late Pleistocene sediments of the Indian Ocean 24–16 ka ago (D. 91 Wall-Palmer personal observation) and in Pliocene rocks of Pangasinan, Philippines 92 [15]. Most of these local extinctions have occurred within the warming period since 93 the Last Glacial Maximum, and may reflect sensitivity to a changing ocean. 94 95 Holoplanktonic gastropods are thought to have evolved from benthic gastropods with 96 planktotrophic larvae, with likely progression to remain planktonic in response to 97 hostile, anoxic bottom conditions [16]. Holoplanktonic gastropods first appear in the 98 Jurassic, likely triggered by the Early Jurassic Anoxia Event [17]. Amongst the 99 earliest holoplanktonic gastropods are several potential heteropod genera including 100 Coelodiscus, Freboldia and Tatediscus [16, 18, 19]. Coelodiscus minutus [16, 20] 101 from the Pliensbachian–Aalenian of the Early–Middle Jurassic (190.8–170.3 Ma) is 102 the earliest known holoplanktonic caenogastropod and probable heteropod. 103 Coelodiscus minutus has a shell morphology remarkably similar to larval atlantid 104 shells of the genus Atlanta (Fig. 2A-D). It is thought that C. minutus does represent 105 an early heteropod [18], but only two ontogenetic stages can be identified from 106 abundant fossil material (compared to three in modern heteropods), and therefore it 107 is not a member of any of the extant families [16]. The planktotrophic larval stage of 108 C. minutus probably became the adult stage when transitioning to a holoplanktonic 109 mode of life, and the adult shell of the modern atlantid heteropods developed later 110 [16]. 111 112 The oldest potential member of the family Atlantidae does not appear in the fossil 113 record until ~57 Ma later, in the Early Cretaceous. Bellerophina minuta [21, 22], 114 found in the Albian (~113–100.5 Ma), has an involute, more rounded shell 115 morphology with clear ornamentation that is similar to larval shells of the extant 116 atlantid genus Oxygyrus (Fig. 2E-H). Destombes [23] considered the relationship 117 between B. minuta and the genus Oxygyrus to be unclear, due to differences in size 118 and incompleteness of the aperture in B. minuta fossils. He therefore placed B. 119 minuta into a separate family, Bellerophinidae, in which an older genus Freboldia 4 120 (163.5–157.3 Ma) is now also placed [17]. However, here we consider B. minuta to 121 belong within the family Atlantidae, having a shell morphology very similar to the 122 extant genus Oxygyrus [22]. Freboldia fluitans (163.5–157.3 Ma) is thought to be 123 holoplanktonic and its shell morphology is involute and quite rounded in shape, 124 however, unlike B. minuta, the shell surface has little or no ornamentation, and the 125 coiling direction of F. fluitans cannot be determined with certainty [17]. 126 127 Through the Late Cretaceous, Paleocene and Eocene there are no known atlantid 128 fossils, creating a gap in the record of ~73 Ma. The recent fossil record of the 129 Atlantidae, extending to the Piacenzian (3.6–0 Ma) is relatively well known [5]. 130 However, from the Piacenzian to the Chattian of the Oligocene (~27.82–3.6 Ma) [24], 131 diversity is much lower with only five atlantid species, and two not determined to 132 species level. There are eight atlantid species known to have become extinct during 133 the Miocene and the Pliocene [5], and one extinct genus, Atlantidea [25]. 134 135 Although heteropods have almost certainly been alive for the last ~190 Ma, nothing is 136 known from these large 57 Ma and 73 Ma gaps in the fossil record, and so the 137 evolutionary diversification patterns and timing of this group are unclear. It has been 138 hypothesised that within the family Atlantidae, the genus Atlanta, with an entirely 139 aragonite shell, is the earliest diverged, and that the genus Oxygyrus, with a shell 140 composed of both aragonite and conchiolin (probably to improve buoyancy), is the 141 most derived [2, 26–29]. However, the shell of the Early Cretaceous B. minuta is 142 morphologically most similar to Oxygyrus (Fig. 2), contradicting this hypothesised 143 evolutionary history of the atlantids. 144 145 Only a single large-scale study has previously explored the molecular phylogeny of 146 the atlantid heteropods [30]. Wall-Palmer et al.[30] revealed considerable hidden 147 diversity using a global dataset of mitochondrial cytochrome c oxidase subunit 1 148 (CO1) sequences from specimens of all known atlantid morphospecies.