An integrative approach to species delimitation in Benthomangelia (Mollusca: Conoidea) Nicolas Puillandre, Michel Baylac, Marie-Catherine Boisselier, Corinne Cruaud, Sarah Samadi To cite this version: Nicolas Puillandre, Michel Baylac, Marie-Catherine Boisselier, Corinne Cruaud, Sarah Samadi. An integrative approach to species delimitation in Benthomangelia (Mollusca: Conoidea). Biological Journal of the Linnean Society, Linnean Society of London, 2009, 96 (3), pp.696-708. 10.1111/j.1095- 8312.2008.01143.x. hal-02458057 HAL Id: hal-02458057 https://hal.archives-ouvertes.fr/hal-02458057 Submitted on 28 Jan 2020 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. Biological Journal of the Linnean Society An integrative approach to species delimitation in Benthomangelia (Mollusca: Conoidea) For Peer Review Journal: Biological Journal of the Linnean Society Manuscript ID: BJLS-0618.R1 Manuscript Type: Original Manuscript Date Submitted by the n/a Author: Complete List of Authors: Puillandre, Nicolas; MNHN, Systematique & Evolution Baylac, Michel; MNHN, UMR 5202 Boisselier, Marie-Catherine; MNHN, UMR 7138 cruaud, corinne; Genoscope samadi, sarah; IRD, MNHN, Dept Syst & Evol 28S rRNA, COI gene, Benthomangelia, DNA taxonomy , Elliptic Keywords: Fourier Analysis , Integrative taxonomy , Molluscs Biological Journal of the Linnean Society Page 1 of 30 Biological Journal of the Linnean Society 1 2 3 4 An integrative approach to species delimitation in Benthomangelia 5 6 (Mollusca: Conoidea) 7 8 9 10 11 N. Puillandre 1,*, M. Baylac 2, M. -C. Boisselier 1, C. Cruaud 3, S. Samadi 1 12 13 14 15 1 16 Université Pierre et Marie Curie (UPMC), UMR 7138, Systématique, adaptation, é volution 17 18 (UPMC /IRD /MNHN /CNRS ), Paris, France. 19 20 2 For Peer Review 21 Muséum national d’Histoire n aturelle (MNHN), USM 0601 Origine, structure et évolution 22 23 de la biodiversité, Paris, France 24 25 3 GENOSCOPE, Centre National de Séquençage, Evry, France 26 27 28 29 30 * Corresponding author: UMR 7138, Systématiqu e, adaptation, évolution, UPMC; IRD; 31 32 33 MNHN; CNRS, Service de systématique moléculaire (CNRS, IFR 101), Département 34 35 systématique et évolution, Muséum National d’Histoire Naturelle, CP26, 57 rue Cuvier, 36 37 75231 Paris Cedex 05, France. ; [email protected] ; +33 1 40 79 37 43 38 39 40 41 42 43 44 Running title: 45 46 47 48 49 Integrative taxonomy in Benthomangelia 50 51 52 53 54 55 56 57 58 59 60 Biological Journal of the Linnean Society Biological Journal of the Linnean Society Page 2 of 30 1 2 3 Abstract 4 5 6 DNA sequences are currently used to propose primary hypotheses of species delimitation, 7 8 especially when morphological variabili ty is difficult to assess. In an integrative taxonomy 9 10 framework, these hypotheses are then compared with other characters, such as morphology or 11 12 13 geography, to produce robust species delimitations. For this purpose, the COI gene has been 14 15 sequenced for almos t 50 specimens of the genus Benthomangelia , a deep -sea marine 16 17 18 gastropod genus, collected in the South -West Pacific. Five genetic groups , displaying low and 19 20 high genetic distances Forrespectively Peer within and betweenReview groups , were defined . COI hypotheses 21 22 were com pared to both the results obtained with the independent nuclear 28S gene and to an 23 24 25 Elliptic Fourier Analysis of the shape of the last whorl of the shell. 28S gene analysis 26 27 confirmed the same well -supported groups as COI, and Elliptic Fourier Analysis ident ified 28 29 several morphological characters that vary similarly to genetic variability . 30 31 32 33 34 35 36 Keywords 37 38 39 28S rRNA - COI gene – Benthomangelia – DNA taxonomy – Elliptic Fourier A nalysis - 40 41 Integrative taxonomy – Molluscs . 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Biological Journal of the Linnean Society Page 3 of 30 Biological Journal of the Linnean Society 1 2 3 Introdu ction 4 5 6 Given the sizeable number of species that remains to be described, especially in the context of 7 8 a rapidly increasing rate of species extinctions, we urgently need to rethink the work of alpha - 9 10 taxonomy to improve the rate of species description. In marine environments, the amount of 11 12 13 unknow n diversity is important , especially for molluscs (Bouchet et al ., 2002 ). Among marine 14 15 molluscs, the Conoidea are one of the most d ivers e taxa (Bouchet , 1990; Taylor , Kantor & 16 17 18 Sysoev, 1993), and it includes a significant portion of undescribed speci es. Morevover, most 19 20 of the described taxaFor from Peershallow water Review and deeper ecosystems remain largely 21 22 underexplored. The difficulty of sampling in such environment and the lac k of specialists for 23 24 25 most of the se groups explain this taxonomic impediment (Boyle et al ., 2004; ). 26 27 Until recently most species descriptions of shelled molluscs were based exclusively on shell 28 29 characters, leading to brief diagnoses that in some cases apply to more than one taxon. 30 31 32 Furthermore, shell variability is difficult to characterize w ith discrete characters (Pfenninger , 33 34 Cordellier & Streit , 2006), and consequently the analysis of s uch characters , as done 35 36 traditionally, is difficult to reproduce . Finally, the broad plasticity of shell characters for some 37 38 39 well known sp ecies was demonstra ted ( Hollander et al ., 2006 ; Brookes & Rochette, 2007 ), 40 41 but this problem is rarely integrated in mollusc taxonomy. For all these reasons, t axonomists 42 43 44 may differ in how they interpret variability of shell characters: what one specialist interprets 45 46 as geogra phical or bathymetrical variation can be interpreted by another as specific 47 48 differences. As a consequence, quite contradictory opinions about species delimitations in 49 50 51 literature are not rare ( e.g. Röckel , Rolan & Monteiro (1980) vs Monteiro, Tenorio & Popp e 52 53 (2004) [Cape Verde Conus ]). 54 55 The difficulty of confronting different opinions is also increased by the lack of a solid 56 57 58 theoretical and methodological framework, de facto rendering many taxonomical opinions 59 60 untestable hypotheses. Recently, concepts and met hods underlying the delimitation of Biological Journal of the Linnean Society Biological Journal of the Linnean Society Page 4 of 30 1 2 3 terminal taxa were clarified, advocat ing for the u se of an integrative framework . De Queiroz 4 5 6 (1998) , followed by Samadi & Barberousse (2006 ), first suggested that a unified view of 7 8 “what is a species” is possible if spec ies are considered as definitively diverging lineages and 9 10 most of the other so -called “species concepts” as criteria for delimiting species (Sites & 11 12 13 Marshall, 2003). In this context, m olecular characters are classica lly used to propose pri mary 14 15 hypothe ses of species delimitation based on genetic distances ( Floyd et al ., 2002 ; Vogler & 16 17 18 Monaghan , 2007) . Contrary to the morphological characters used in most mollusc species 19 20 description, molecularFor characters Peerare strictly heritable Review and reproducible. Within an integrative 21 22 framework (De Queiroz, 2007) these primary molecular hypothese s can then be tested against 23 24 25 several criteria , namely : (i) monophyly of primary species hypotheses (Wheeler & Meier, 26 27 2000 ; Meyer & Paulay , 200 5), (ii) independ ent genetic marker s, s uch as a nuclear gene , as 28 29 gene tree s do not necessar ily reflect the species tree ( Nichols , 2001 ; Funk & Omland , 2003 ), 30 31 32 and (iii) morphological analysis to discuss species delimitations based on genetic data 33 34 (Bichain et al ., 2007 ; Pfenninger et al ., 2006) . 35 36 In this integrative context , we aim to combine several criteria to propose new hypothese s of 37 38 39 spe cies delimitations in the genus Benthomangelia (Conoidea , Conidae ). This is a widely 40 41 distributed genus of bathyal and abyssal marine molluscs (Bouchet & War én, 1980) . It was 42 43 44 described by Thiel e ( 1925 ), grouping together species previously placed in other genera . 45 46 Since 1925 , new species have been described , based on morphological characters such as 47 48 orna mentations and shape of the shell (Bouchet & War én, 1980; Syso ev & Ivanov , 1985; 49 50 51 Sysoev , 1988) . Ten species are now considered as valid (Tucker 2004) , of which six are 52 53 present in the Pacific . Several potential new forms have been recently collected during cruises 54 55 organized by the Museum National d’Histoire Naturelle (MNHN) and the Institut de 56 57 58 Recherche pour le Développement (IRD) , but the great and sometimes continuous 59 60 Biological Journal of the Linnean Society Page 5 of 30 Biological Journal of the Linnean Society 1 2 3 morphological variability complicat e the delimitation of species based solely on th ese 4 5 6 characters (Bouchet & Sysoev , 2001) . 7 8 We demonstrate the delimit ation of genetic groups within the genus Benthomangelia , using 9 10 molecular characters and a tree -based method . Two independe nt genes are used, one 11 12 13 mitochondrial (COI) and one nuclear (28S ) gene . An E lliptic Fourier Analysis ( EFA; Rohlf , 14 15 1996) of the shape of the last whorl of the shell is also performed, allowing detailed analysis 16 17 18 of comp lex structures as a whole (Monti, Baylac & Lalanne -Cassou , 2001).