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Neogastropoda, Conoidea) Jawad Abdelkrim, Laetitia Aznar-Cormano, Alexander Fedosov, Yuri Kantor, Pierre Lozouet, Mark Phuong, Paul Zaharias, Nicolas Puillandre

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Neogastropoda, Conoidea) Jawad Abdelkrim, Laetitia Aznar-Cormano, Alexander Fedosov, Yuri Kantor, Pierre Lozouet, Mark Phuong, Paul Zaharias, Nicolas Puillandre Exon-Capture-Based Phylogeny and Diversification of the Venomous Gastropods (Neogastropoda, Conoidea) Jawad Abdelkrim, Laetitia Aznar-Cormano, Alexander Fedosov, Yuri Kantor, Pierre Lozouet, Mark Phuong, Paul Zaharias, Nicolas Puillandre To cite this version: Jawad Abdelkrim, Laetitia Aznar-Cormano, Alexander Fedosov, Yuri Kantor, Pierre Lozouet, et al.. Exon-Capture-Based Phylogeny and Diversification of the Venomous Gastropods (Neogastropoda, Conoidea). Molecular Biology and Evolution, Oxford University Press (OUP), 2018, 35 (10), pp.2355- 2374. hal-02002406 HAL Id: hal-02002406 https://hal.archives-ouvertes.fr/hal-02002406 Submitted on 31 Jan 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. 1 Manuscript type: Article/Discoveries 2 3 4 Exon-capture based phylogeny and diversification of the venomous gastropods 5 (Neogastropoda, Conoidea). 6 7 Abdelkrim J.1, Aznar-Cormano L.1, Fedosov A.2, Kantor Y.2, Lozouet P.3, Phuong M.4, 8 Zaharias P.5, Puillandre N.5 9 10 1 UMS 2700, Museum National d’Histoire Naturelle, Département Systématique et Evolution, 11 43, Rue Cuvier, 75231 Paris, France 12 2 A.N. Severtzov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninski 13 prospect 33, 119071 Moscow, Russian Federation 14 3 Department of Ecology and Evolutionary Biology, University of California, Los Angeles, 15 CA 90095, USA 16 4 Muséum national d’Histoire naturelle, 55 rue de Buffon, F-75005 Paris 17 5 Institut Systématique Evolution Biodiversité (ISYEB), Muséum national d'Histoire 18 naturelle, CNRS, Sorbonne Université, EPHE, 57 rue Cuvier, CP 26, 75005 Paris, France. 19 20 Corresponding author: Nicolas Puillandre, [email protected] 21 22 ABSTRACT 23 24 Transcriptome-based exon capture methods provide an approach to recover several hundred 25 markers from genomic DNA, allowing for robust phylogenetic estimation at deep timescales. 26 We applied this method to a highly diverse group of venomous marine snails, Conoidea, for 27 which published phylogenetic trees remain mostly unresolved for the deeper nodes. We 28 targeted 850 protein coding genes (678,322 base pairs) in ca. 120 samples, spanning all 29 (except one) known families of Conoidea and a broad selection of non-Conoidea 30 neogastropods. The capture was successful for most samples, although capture efficiency 31 decreased when DNA libraries were of insufficient quality and/or quantity (dried samples or 32 low starting DNA concentration) and when targeting the most divergent lineages. An average 33 of 75.4% of proteins was recovered, and the resulting tree, reconstructed using both 34 supermatrix (IQ-tree) and supertree (Astral-II, combined with the Weighted Statistical 35 Binning method) approaches, are almost fully supported. A reconstructed fossil-calibrated 36 tree dates the origin of Conoidea to the Lower Cretaceous. We provide descriptions for two 37 new families. The phylogeny revealed in this study provides a robust framework to re- 38 interpret changes in Conoidea anatomy through time. Finally, we used the phylogeny to test 39 the impact of the venom gland and radular type on diversification rates. Our analyses revealed 40 that repeated losses of the venom gland had no effect on diversification rates, while families 41 with a breadth of radula types showed increases in diversification rates, thus suggesting that 42 trophic ecology may have an impact on the evolution of Conoidea. 43 44 INTRODUCTION 45 Next-generation sequencing (NGS) techniques have enabled the resolution of deep 46 phylogenetic relationships by facilitating the rapid acquisition of genetic markers across 47 divergent taxa (Lemmon and Lemmon 2013; McCormack et al. 2013). This field of research 48 has been particularly active for non-model organisms, for which genomic and transcriptomic 49 data are scarce (Bi et al. 2012; Cariou et al. 2013; da Fonseca et al. 2016; Yeates et al. 2016). 50 In molluscs, a major bottleneck in applying NGS techniques has been the identification of 51 suitable markers for phylogenetic inference (Schrödl and Stöger 2014). As such, phylogenetic 52 analyses applying NGS techniques have been limited to mitogenomes (e.g., Osca et al. 2015; 53 Lee et al. 2016), transcriptome sequencing (e.g., Kocot et al. 2011; Smith et al. 2011; Zapata 54 et al. 2014; González et al. 2015; Tanner et al. 2017) or RAD-sequencing (e.g., Combosch et 55 al. 2017). While they provided better-resolved phylogenetic trees compared to the traditional 56 Sanger sequencing of a few mitochondrial and nuclear genes, each have their own limitations. 57 For example, resulting trees can be potentially biased when only mitochondrial data are used 58 (Platt et al. 2017). Further, transcriptome-based approaches need RNA-preserved samples and 59 the associated costs may be prohibitive to laboratories with more limited budgets. 60 Transcriptome based exon capture methods provide an approach to recover hundreds 61 of genetic markers from genomic DNA, allowing for robust phylogenetic estimation and does 62 not rely on RNA-preserved or fresh samples (Bi et al. 2012; Hugall et al. 2015; Teasdale et al. 63 2016). Furthermore, because it targets short DNA fragments (typically between 100 bp and 64 400bp), older specimens that were not preserved in ideal conditions for molecular analysis 65 can also be sequenced. In molluscs, 250 years of taxonomy based on shell collecting have 66 cataloged and preserved an impressive amount of material. Although molluscs are 67 traditionally preserved dried (Bouchet and Strong 2010), recent efforts in the framework of 68 the “La Planète Revisitée” and the “Tropical Deeps-Sea Benthos” expedition programs 69 (http://expeditions.mnhn.fr) have amassed a large collection of alcohol-preserved samples. 70 The high quantity of dry and alcohol preserved material, together with their huge species 71 diversity, the lack of genomic data and the ease of generating transcriptome data, makes 72 Mollusca a good model to test the applicability of the exon-capture approach to non-model 73 organisms. 74 Conoidea is a group of hyperdiverse venomous gastropods (5,000 described species 75 for a total estimated around 10–20,000 – Bouchet et al. 2009), distributed across all oceans, 76 latitudes, and depths. Conoideans, and in particular cone snails, are one of the most studied 77 groups of animals for the toxins they produce. These toxins are highly diversified and 78 specific, and some of them are used – or about to be used – as therapeutics (Prashanth et al. 79 2014). In a series of articles, several molecular phylogenies were published (Puillandre et al. 80 2008; Puillandre et al. 2011) followed by subsequent descriptions of new families and the 81 publication of a new classification (Bouchet et al. 2011; Kantor et al. 2012) that were deeply 82 modified compared to the previous classifications. These phylogenies included a 83 representative (although not complete) sampling of the superfamily diversity (WORMS 84 2018). However, these phylogenies are all based on a few Sanger-sequenced markers, 85 typically the mitochondrial COI (cytochrome c oxidase subunit I), 16S rRNA and 12S rRNA 86 genes and the nuclear 28S rRNA, 18S rRNA and histone H3 genes. While the analyses of 87 these loci recognized clades from the species to family levels (i.e. up to 50 MYA, roughly), 88 their resolving power was limited as they were unable to define older relationships. 89 Researchers working on conoideans now have a phylogenetic classification for the group, but 90 understanding the processes underlying the evolutionary success of the group and of the 91 toxins they produce requires a better resolved phylogenetic tree. Recently, Uribe et al. 92 (2018)proposed a phylogeny based on full mitogenomes, and while it was more resolved 93 compared to previously published trees, sampling of conoidean diversity was still limited. 94 Here, we aim to generate the most complete and resolved phylogeny of Conoidea published 95 so far, including representatives of most of the known family-level lineages by applying an 96 exon-capture strategy to target thousands of loci. We explored several approaches of tree 97 reconstructions designed for very large datasets. We also identified, for the first time, several 98 fossils that can be attributed to the molecularly-defined lineages and used these fossils to 99 reconstruct a time-calibrated tree. The obtained phylogeny is almost fully resolved and 100 supported, reveals new family-level lineages of conoideans and unexpected phylogenetic 101 relationships between the families, and modifies some of the traditionally well-defined groups 102 within the superfamily. Such phylogenies can then be used as a framework to test hypotheses 103 related to the evolutionary success of the group. To illustrate this idea, we analyzed the 104 variability of the diversification rates among conoidean families and tested the relationships 105 between diversification rates and the evolution of two traits (venom gland and radula) related 106 to the venom apparatus, a structure thought to contribute to the evolutionary success of the 107 conoideans. 108 109 110 RESULTS 111 112 Exon capture 113 We used available Conoidean transcriptome data from the literature and online 114 resources to identify 850 protein coding genes. We tentatively captured 120 samples 115 representing the diversity of the Conoidea, as well as a selection of non-conoidean 116 neogastropod lineages. Two samples failed at the library preparation step (because of very 117 low quantity of DNA available) and were thus not sequenced: the unique sample of 118 Bouchetispiridae and an unidentified turrid, “HORS_MNHN_Stahlschmidt_9”.
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