Abstract
The evolutionary relationships of the nudibranch genus Dondice Er. Marcus, 1958, its hypothesized synonym with Nanuca Er. Marcus, 1957, as well as its species-level diversity remain unresolved. Here, in order to assess the systematics of Dondice a molecular phylogenetic analysis based on cytochrome c oxidase I and 16S genes was carried out, including various representatives of the Myrrhinidae. As a result, Dondice is monophyletic and a valid genus, presenting morphological diagnostic features when compared to Nanuca. An integrative taxonomic approach focused on Western Atlantic Dondice occidentalis (Engel, 1925) and Dondice parguerensis Brandon & Cutress, 1985, including a broader geographic and morphological range of specimens, indicates that D. occidentalis constitutes a complex of six pseudocryptic species with geographically restricted ranges across the Western Atlantic, and D. parguerensis is a distinct, valid species. Dondice occidentalis s. str. is recognized as the species of the genus with the largest morphological variation, whereas the five new species, Dondice arianeae sp. nov., Dondice freddiemercuryi sp. nov., Dondice juansanchezi sp. nov., Dondice jupiteriensis sp. nov., and Dondice caboensis sp. nov. exhibit consistent morphological patterns, in agreement with molecular distinctiveness. Our study increases the number of known species of Dondice from four to nine and highlights the importance of addressing marine biodiversity within an integrative framework.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Agudo-Padrón AI, Bleicker MS, Saafeld K (2009) Recent marine molluscs of Santa Catarina state, SC, southern Brazil region: a comprehensive synthesis and check list. VISAYA Net 3:1–17
Akaike H (1974) A new look at the statistical model identifications. IEEE Trans Automat Contr 19:716–723
Álvarez-Campos P, Giribet G, Riesgo A (2017) The Syllis gracilis species complex: a molecular approach to a difficult taxonomic problem (Annelida, Syllidae). Mol Phylogenet Evol 109:138–150. https://doi.org/10.1016/j.ympev.2016.12.036
Anthes N, Michiels NK (2004) Do “sperm trading” simultaneous hermaphrodites always trade sperm? Behav Ecol 16:188–195. https://doi.org/10.1093/beheco/arh150
Anthes N, Putz A, Michiels NK (2005) Gender trading in a hermaphrodite. Curr Biol 15:R792–R793. https://doi.org/10.1016/j.cub.2005.09.035
Anthes N, Schulenburg H, Michiels NK (2008) Evolutionary links between reproductive morphology, ecology and mating behavior in opisthobranch gastropods. Evol: Int J Org Evol 62:900–916. https://doi.org/10.1111/j.1558-5646.2008.00326.x
Ardila NE, Báez DP, Valdés A (2007) Babosas y liebres de mar (Mollusca: Gastropoda: Opisthobranchia) de Colombia. Biota Colomb 8:185–197
Baba K (1930) Studies on Japanese Nudibranchs (3): A. Phyllidiidae: Studies on Japanese Nudibranchs (3): B. Aeolididae. The Venus 2:117–125
Baba K, Hamatani I (1965) The anatomy of Sakuraeolis enosimensis (Baba, 1930), n. g. (= Hervia ceylonica (?) Eliot, 1913) (Nudibranchia-Eolidoidea). Publ Seto Mar Biol Lab 13:103–113
Bandel K (1976) Egg masses of 27 Caribbean opisthobranchs from Santa Marta, Columbia. Stud Neotrop Fauna Environ 11:87–118
Barroso R, Klautau M, Solé-Cava AM, Paiva PC (2010) Eurythoe complanata (Polychaeta: Amphinomidae), the ‘cosmopolitan’ fireworm, consists of at least three cryptic species. Mar Biol 157:69–80
Barroso CX, de Freitas JEP, Matthews-Cascon H, Bezerra LEA, da Cruz Lotufo TM (2020) Molecular evidences confirm the taxonomic separation of two sympatric congeneric species (Mollusca, Gastropoda, Neritidae, Neritina). ZooKeys 904:117–130. https://doi.org/10.3897/zookeys.904.46790
Beninger PG, Valdizan A, Le Pennec G (2016) The seminal receptacle and implications for reproductive processes in the invasive gastropod Crepidula fornicata. Zool 119:4–10. https://doi.org/10.1016/j.zool.2015.09.001
Bergh R (1879) On the nudibranchiate grastropod Mollusca of the North Pacific Ocean, with special reference to those of Alaska. Proc Acad Nat Sci Philadelphia 2:71–132
Bergh LSR (1867) Phidiana lynceus og Ismaila monstrosa. Vidensk. Meddel. Naturhist. Foren 7:97–130
Bergh LSR (1889) Opisthobranchia. In: Carus JV (ed) Prodromus faunae Mediterraneae sive descriptio animalium maris mediterranei incolarum quam comparata silva rerum quatenus innotuit adiectic locis et nominibus vulgaribus eorumque auctoribus in commodum zoologorum congessit Julius Victor Carus. Schweizerbart'sch Verlagshandlund, Stuttgart, pp. 183–232
Bergh LSR (1905) Die Opisthobranchiata der Siboga-expedition. Siboga-Expeditie 50:1–248
Bharate M, Padula V, Apte D, Shimpi GG (2020) Integrative description of two new Cratena species (Mollusca: Nudibranchia) from western India. Zootaxa 4729:359–370. https://doi.org/10.11646/zootaxa.4729.3.4
Bird CE, Fernandez-Silva I, Skillings DJ, Toonen RJ (2012) Sympatric speciation in the post “modern synthesis” era of evolutionary biology. Evol Biol 39:158–180
Bowen BW, Rocha LA, Toonen RJ, Karl SA (2013) The origins of tropical marine biodiversity. Trends Eco Evo 28:359–366
Brandon M, Cutress CE (1985) A new Dondice (Opisthobranchia: Favorinidae), predator of Cassiopea in Southwest Puerto Rico. Bull Mar Sci 36:139–144
Caballer-Gutierrez M, Ortea J, Rivero N, Tucker GC, Malaquias MAE, Narciso S (2015) The opisthobranch gastropods (Mollusca: Heterobranchia) from Venezuela: an annotated and illustrated inventory of species. Zootaxa 4034:201–256. https://doi.org/10.11646/zootaxa.4034.2.1
Calvo M, Templado J, Oliverio M, Machordom A (2009) Hidden Mediterranean biodiversity: molecular evidence for a cryptic species complex within the reef building vermetid gastropod Dendropoma petraeum (Mollusca: Caenogastropoda). Biol J Linn Soc 96:898–912. https://doi.org/10.1111/j.1095-8312.2008.01167.x
Carmona L, Lei BR, Pola M, Gosliner TM, Valdés A, Cervera JL (2014) Untangling the Spurilla neapolitana (Delle Chiaje, 1841) species complex: a review of the genus Spurilla Bergh, 1864 (Mollusca: Nudibranchia: Aeolidiidae). Zool J Linnean Soc 170:132–154. https://doi.org/10.1111/zoj12098
Carstens BC, Pelletier TA, Reid NM, Satler JD (2013) How to fail at species delimitation. Mol Ecol 22:4369–4383. https://doi.org/10.1111/mec.12413
Chollett I, Mumby PJ, Müller-Karger FE, Hu C (2012) Physical environments of the Caribbean Sea. Limnol Oceanogr 57:1233–1244. https://doi.org/10.4319/lo.2012.57.4.1233
Churchill CK, Alejandrino A, Valdés A, Foighil DÓ (2013) Parallel changes in genital morphology delineate cryptic diversification of planktonic nudibranchs. Proc R Soc B 280:20131224. https://doi.org/10.1098/rspb.2013.1224
Churchill CK, Valdés Á, Foighil DÓ (2014) Molecular and morphological systematics of neustonic nudibranchs (Mollusca: Gastropoda: Glaucidae: Glaucus), with descriptions of three new cryptic species. Invertebr Syst 28:174–195. https://doi.org/10.1071/IS13038
Clark KB, Goetzfried A (1978) Zoogeographic influences on development patterns of North Atlantic Ascoglossa and Nudibranchia, with a discussion of factors affecting egg size and number. J Molluscan Stud 44:283–294. https://doi.org/10.1093/oxfordjournals.mollus.a065435
Clelland E, Di Renna T, Saleuddin ASM (2001) The structure of the bursa copulatrix in virgin and mated snails, Helisoma duryi (Mollusca): role of acid phosphatase in reproduction. Invertebr Biol 120:1–12. https://doi.org/10.1111/j.1744-7410.2001.tb00021.x
Collin R, Díaz MC, Norenburg J, Rocha RM, Sánchez JA, Shulze A, Schwartz M, Valdés Á (2005) Photographic identification guide to some common marine invertebrates of Bocas del Toro, Panama. Caribb J Sci 41:638–707
Couthouy JP (1838) Descriptions of new species of Mollusca and shells, and remarks on several polypii, found in Massachussets Bay. Boston J Nat Hist 2:53–111
Cowen RK, Paris CB, Srinivasan A (2006) Scaling of connectivity in marine populations. Science 311:522–527. https://doi.org/10.1126/science.1122039
Cubit JD, Williams S (1983) The invertebrates of Galeta reef (Caribbean Panama): a species list and bibliography. Atoll Res Bull 269:1–45
Cuvier GLCF (1817) Le règne animal distribué d'après son organisation: pour servir de base a l'histoire naturelle des animaux et d'introduction a l'anatomie compare. Déterville, Paris
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
De Queiroz K (2007) Species concepts and delimitation. Syst Biol 56:879–886. https://doi.org/10.1080/10635150701701083
Dellicour S, Flot JF (2015) Delimiting species-poor data sets using single molecular markers: a study of barcode gaps, haplowebs and GMYC. Syst Biol 64:900–908. https://doi.org/10.1093/sysbio/syu130
Dias RM, Lima SM, Mendes LF, Almeida DF, Paiva PC, Britto MR (2019) Different speciation processes in a cryptobenthic reef fish from the Western tropical Atlantic. Hydrobiol 837:133–147. https://doi.org/10.1007/s10750-019-3966-z
Eberhard W (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, New Jersey
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Edmunds M (1964) Eolid Mollusca from Jamaica, with descriptions of two new genera and three new species. Bull Mar Sci 14:1–32
Ehrenberg CG (1831) Symbolae physicae seu icones et descriptiones animalium evertebratorum sepositis insectis quae ex itinere per Africam borealem et Asiam. Officina Academia, Berolini
Ehrenberg CG (1834) Beiträge zur physiologischen Kenntniss der Corallenthiere im allgemeinen, und besonders des rothen Meeres, nebst einem Versuche zur physiologischen Systematik derselben. Abh Konigl Akad Wiss Berlin 1:225–380
Ekimova I, Valdés Á, Chichvarkhin A, Antokhina T, Lindsay T, Schepetov D (2019) Diet-driven ecological radiation and allopatric speciation result in high species diversity in a temperate-cold water marine genus Dendronotus (Gastropoda: Nudibranchia). Mol Phylogenet Evol 141:106609. https://doi.org/10.1016/j.ympev.2019.106609
Engel H (1925) Westindische opisthobranchiate Mollusken. Bijdragen tot de kennis der fauna van Curaçao. Resultaten eener reis van Dr. C. J. van der Horst in 1920. Bijdr Dierkd 24:33–80
Espinosa J, Ortea J (2001) Moluscos del mar Caribe de Costa Rica: desde Cahuita hasta Gandoca. Mollusca of Costa Rica Caribbean Sea: from Cahuita to Gandoca Avicennia 4:1–20
Espinosa J, Ortea J, Caballer M, Moro L (2006) Moluscos marinos de la península de Guanahacabibes, Pinar del Río, Cuba, con la descripción de nuevos taxones. Avicennia 18:1–83
Evanno G, Madec L, Arnaud JF (2005) Multiple paternity and postcopulatory sexual selection in a hermaphrodite: what influences sperm precedence in the garden snail Helix aspersa? Mol Ecol 14:805–812. https://doi.org/10.1111/j.1365-294X.2005.02449.x
Eyster LS (1980) Distribution and reproduction of shell-less opisthobranchs from South Carolina. Bull Mar Sci 30:580–599
Ezard T, Fujisawa T, Barraclough T (2017) SPLITS: species’ limits by threshold statistics. R package version 1.0-19/r52. Available at: https://R-Forge.R-project.org/projects/splits/
Faucci A, Toonen RJ, Hadfield MG (2007) Host shift and speciation in a coral-feeding nudibranch. Proc R Soc B 274:111–119. https://doi.org/10.1098/rspb.2006.3685
Ferreira-Jr A, Wambier S, Carvalho I, Absher T (2015) New records of marine “sea slugs” (Mollusca: Gastropoda: Heterobranchia) in the outlets of the estuary systems in Paraná, southern Brazil. Check List 11:1–4. https://doi.org/10.15560/11.1.1548
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the generalized mixed yule coalescent (GMYC) approach: a revised method and evaluation on simulated datasets. Syst Biol 44:1–49. https://doi.org/10.1093/sysbio/syt033
Furfaro G, Mariottini P (2020) A new Dondice Marcus Er. 1958 (Gastropoda: Nudibranchia) from the Mediterranean Sea reveals interesting insights into the phylogenetic history of a group of Facelinidae taxa. Zootaxa 4731:001–022. https://doi.org/10.11646/zootaxa.4731.1.1
Furfaro G, Mariottini P (2021a) Looking at the nudibranch family Myrrhinidae (Gastropoda, Heterobranchia) from a mitochondrial ‘2D folding structure’ point of view. Life 11:583. https://doi.org/10.3390/life11060583
Furfaro G, Mariottini P (2021b) Nemesignis, a replacement name for Nemesis Furfaro & Mariottini, 2021 (Mollusca, Gastropoda, Myrrhinidae), preoccupied by nemesis Risso, 1826 (Crustacea, Copepoda). Life 11:809. https://doi.org/10.3390/life11080809
Furfaro G, Modica MV, Oliverio M, Mariottini P (2016) A DNA-barcoding approach to the phenotypic diversity of Mediterranean species of Felimare Ev. Marcus & Er. Marcus, 1967 (Mollusca: Gastropoda), with a preliminary phylogenetic analysis. Italian J Zool 83:195–207. https://doi.org/10.1080/11250003.2016.1150525
Galvão-Filho HC, Araújo AK, Silva FV, Azevedo VM, Meirelles CA, Matthews-Cascon H (2015) Sea slugs (Gastropoda: Heterobranchia) from a poorly known area in north-East Brazil: filling gaps in Atlantic distributions. Mar Biodivers Rec 8:e115. https://doi.org/10.1017/S1755267215000494
García JC, García FJ (1984) Estudio anatómico y algunas reseñas ecológicas de Godiva banyulensis (Portmann y Sandmeir)(Gastropoda: Nudibranchia). Cahiers Biol Mar 25:49–65
Golestani H, Crocetta F, Padula V, Camacho-García Y, Langeneck J, Poursanidis D, Pola M, Baki Yokes M, Cervera JL, Jung DW, Gosliner TM, Araya JF, Hooker Y, Schrödl M, Valdés A (2019) The little Aplysia coming of age: from one species to a complex of species complexes in Aplysia parvula (Mollusca: Gastropoda: Heterobranchia). Zool J Linnean Soc 187:279–330. https://doi.org/10.1093/zoolinnean/zlz028
Gonzalez L, Hanson D, Valdés A (2013) Molecular divergence between two sympatric species of Dondice (Mollusca: Nudibranchia) with distinct feeding specializations. J Mar Biol Assoc UK 93:1887–1893. https://doi.org/10.1017/S0025315413000465
Goodheart JA, Bely AE (2017) Sequestration of nematocysts by divergent cnidarian predators: mechanism, function, and evolution. Invert Biol 136:75–91. https://doi.org/10.1111/ivb.12154
Goodheart JA, Bazinet AL, Valdés Á, Collins AG, Cummings MP (2017) Prey preference follows phylogeny: evolutionary dietary patterns within the marine gastropod group Cladobranchia (Gastropoda: Heterobranchia: Nudibranchia). BMC Evol Biol 17:221. https://doi.org/10.1186/s12862-017-1066-0
Goodheart JA, Ellingson RA, Vital X, Galvão Filho HC, McCarthy JB, Medrano SM, Bhave VJ, García-Méndez K, Jiménez LM, López G, Hoover CA, Awbrey JD, De Jesus JM, Gowacki W, Krug PJ, Valdés Á (2016) Identification guide to the heterobranch sea slugs (Mollusca: Gastropoda) from Bocas del Toro, Panama. Mar Biodivers Rec 9:56. https://doi.org/10.1186/s41200-016-0048-z
Grune Loffler S, Crescini R, de Sisto M, Velasquez M, Villalba W (2014) Opistobranquios del Parque Nacional Laguna de La Restinga, Isla de margarita, Venezuela. Amici Molluscarum 22:25–35
Haas F (1920) Opisthobranchier aus verschiedenen warmen Meeren. Archiv für Molluskenkunde 52:138–142
Hess DF, Abbott RT, Hanlon RT, Hamann J, Meyer K, Millen S, Gosliner TM (1994) Marine molluscs of the Cayman Islands. In: Brunt MA, Davies JE (eds) The Cayman Islands, natural history and biogeography. Springer, Netherlands, pp 139–189
Huelsenbeck JP, Rannala B (2004) Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Syst Biol 53:904–913. https://doi.org/10.1080/10635150490522629
ICZN (1999) International code of zoological nomenclature. International Trust for Zoological Nomenclature, London
Jörger KM, Schrödl M (2013) How to describe a cryptic species? Practical challenges of molecular taxonomy. Front Zool 10:59. https://doi.org/10.1186/1742-9994-10-59
Katouzian AR, Sari A, Macher JN, Weiss M, Saboori A, Leese F, Weigand AM (2016) Drastic underestimation of amphipod biodiversity in the endangered Irano-Anatolian and Caucasus biodiversity hotspots. Sci Rep 6:22507. https://doi.org/10.1038/srep22507
Kawauchi GY, Giribet G (2014) Sipunculus nudus Linnaeus, 1766 (Sipuncula): cosmopolitan or a group of pseudo-cryptic species? An integrated molecular and morphological approach. Mar Ecol 35:478–491. https://doi.org/10.1111/maec.12104
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kienberger K, Carmona L, Pola M, Padula V, Gosliner TM, Cervera JL (2016) Aeolidia papillosa (Linnaeus, 1761) (Mollusca: Heterobranchia: Nudibranchia), single species or a cryptic species complex? A morphological and molecular study. Zool J Linnean Soc 177:481–506. https://doi.org/10.1111/zoj.12379
Korshunova T, Mehrotra R, Arnold S, Lundin K, Picton B, Martynov A (2019) The formerly enigmatic Unidentiidae in the limelight again: a new species of the genus Unidentia from Thailand (Gastropoda: Nudibranchia). Zootaxa 4551:556–570. https://doi.org/10.11646/zootaxa.4551.5.4
Krug PJ (2011) Patterns of speciation in marine gastropods: a review of the phylogenetic evidence for localized radiations in the sea. Am Malacol Bull 29:169–187. https://doi.org/10.4003/006.029.0210
Krug PJ, Vendetti JE, Valdés Á (2016) Molecular and morphological systematics of Elysia Risso, 1818 (Heterobranchia: Sacoglossa) from the Caribbean region. Zootaxa 4148:1–137. https://doi.org/10.11646/zootaxa.4148.1.1
Krug PJ, Berriman JS, Valdés Á (2018) Phylogenetic systematics of the shelled sea slug genus Oxynoe Rafinesque, 1814 (Heterobranchia: Sacoglossa), with integrative descriptions of seven new species. Invertebr Syst 32:950–1003. https://doi.org/10.1071/IS17080
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Lamouroux JVF (1812) Extrait d’un mémoire Sur la classification des polypiers coralligènes non entièrement pierreux. N Bull Soc Phil Paris 3:181–188
Lamy D, Pointier JP (2017) Marine and freshwater molluscs of the French Caribbean. PLB Éditions, Le Gosier, Guadalupe
Layton KK, Carvajal JI, Wilson NG (2020) Mimicry and mitonuclear discordance in nudibranchs: new insights from exon capture phylogenomics. Ecol Evol 10:11966–11982. https://doi.org/10.1002/ece3.6727
Lefébure T, Douady CJ, Gouy M, Gibert J (2006) Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Mol Phylogenet Evol 40:435–447. https://doi.org/10.1016/j.ympev.2006.03.014
Ludt WB, Rocha LA (2015) Shifting seas: the impacts of Pleistocene Sea-level fluctuations on the evolution of tropical marine taxa. J Biogeogr 42:25–38. https://doi.org/10.1111/jbi.12416
Lyons WG (1998) Checklist of shallow-water marine Mollusca of Florida. In: Camp DK, Lyons WG, Perkins TH (eds) Florida Department of Environmental Protection Technical Report, TR-3’. Florida Marine Research Institute, Florida, USA, pp 5–78
Macnae W (1954) On some eolidacean nudibranchiate molluscs from South Africa. Annals Natal Mus 13:1–50
Maddison WP, Knowles LL (2006) Inferring phylogeny despite incomplete lineage sorting. Syst Biol 55:21–30. https://doi.org/10.1080/10635150500354928
Magenta-da-Cunha C (2000) Dondice cf. occidentalis from Brasil (Jun 12). [message in] sea slug forum. Australian Museum, Sydney. Available at http://www.seaslugforum.net/find/2547
Malaquias MAE (2014) New data on the heterobranch gastropods (‘opisthobranchs’) for the Bahamas (tropical western Atlantic Ocean). Mar Biodivers Rec 7:e27. https://doi.org/10.1017/S175526721400030X
Marcus Er (1957) On Opisthobranchia from Brazil 2. J Linn Soc London Zool 43:390–486. https://doi.org/10.1111/j.1096-3642.1957.tb01559.x
Marcus Er (1958) On Western Atlantic opisthobranchiate gastropods. Am Mus Novit 1906:1–82
Marcus Er (1961) Opisthobranchia from North Carolina. J Elisha Mitchell Sci Soc 77:141–151
Marcus Ev (1976) Opisthobranchia von Santa Marta, Colombia. Stud Neotrop Fauna Environ 11:119–150
Marcus Er, Marcus Ev (1970) Opisthobranchs from Curaçao and faunistically related regions. Stud Fauna Curaçao other Caribb Isl 33:1–129
Marcus Ev, Marcus Er (1960) Opisthobranchs from American Atlantic warm waters. Bull Mar Sci Gulf Caribb 10:129–203
Marcus Ev, Marcus Er (1967) Some opisthobranchs from Sapelo Island, Georgia. U S A Malacologia 6:199–222
Mariño J, Farfán E, Caballer M (2011) Primer Registro de Dondice parguerensis (Mollusca: Favorinidae) Para Venezuela. Rev Mex Biodivers 82:709–712
Martynov A, Mehrotra R, Chavanich S, Nakano R, Kashio S, Lundin K, Picton B, Korshunova T (2019) The extraordinary genus Myja is not a tergipedid, but related to the Facelinidae s. str. With the addition of two new species from Japan (Mollusca, Nudibranchia). ZooKeys 818:89–116. https://doi.org/10.3897/zookeys.818.30477
Mathews LM, Schubart CD, Neigel JE, Felder DL (2002) Genetic, ecological, and behavioural divergence between two sibling snapping shrimp species (Crustacea: Decapoda: Alpheus). Mol Ecol 11:1427–1437. https://doi.org/10.1046/j.1365-294X.2002.01539.x
McDonald GR, Nybakken JW (1997) List of the worldwide food habits of nudibranchs. Veliger 40:157–1599
Millen S, Hermosillo A (2012) Three new species of aeolid nudibranchs (Opisthobranchia) from the Pacific coast of Mexico, Panama, and the Indopacific, with a redescription and redesignation of a fourth species. Veliger 51:145–164
Monaghan MT, Wild R, Elliot M, Fujisawa T, Balke M, Inward DJ, Vogler AP (2009) Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Syst Biol 58:298–311. https://doi.org/10.1093/sysbio/syp027
Morard R, Quillévéré F, Escarguel G, Ujiie Y, de Garidel-Thoron T, Norris RD, de Vargas C (2009) Morphological recognition of cryptic species in the planktonic foraminifer Orbulina universa. Mar Micropaleontol 71:148–165. https://doi.org/10.1016/j.marmicro.2009.03.001
Moura RL, Amado-Filho GM, Moraes FC, Brasileiro PS, Salomon PS, Mahiques MM, Bastos AC, Almeida MG et al (2016) An extensive reef system at the Amazon River mouth. Sci Advan 2:e1501252. https://doi.org/10.1126/sciadv.1501252
Nauer F, Cassano V, Oliveira MC (2015) Description of Hypnea pseudomusciformis sp. nov, a new species based on molecular and morphological analyses, in the context of the H. musciformis complex (Gigartinales, Rhodophyta). J Appl Phycol 27:2405–2417. https://doi.org/10.1007/s10811-014-0488-y
Ornelas-Gatdula E, Valdés Á (2012) Two cryptic and sympatric species of Philinopsis (Cephalaspidea: Aglajidae) in the Bahamas distinguished using molecular and anatomical data. J Molluscan Stud 78:313–320. https://doi.org/10.1093/mollus/eys022
Ornelas-Gatdula E, Camacho-García Y, Schrödl M, Padula V, Hooker Y, Gosliner TM, Valdés Á (2012) Molecular systematics of the ‘Navanax aenigmaticus’ species complex (Mollusca, Cephalaspidea): coming full circle. Zool Scripta 41:374–385. https://doi.org/10.1111/j.1463-6409.2012.00538.x
Ortea J, Martinez E, Villani G (1994) Estudio comparado de animales de Nanuca sebastiani Marcus, 1957 (Mollusca: Nudibranchia: Aeolidacea) recolectados en aguas de Cuba y Brasil. Avicennia 1:131–136
Ortea J, Espinosa J, Buske Y, Caballer M (2013) Additions to the inventory of the sea slugs (Opisthobranchia and Sacoglossa) from Guadeloupe (Lesser Antilles, Caribbean Sea). Rev Acad Canaria Cienc 25:163–194
Ortigosa D, Lemus-Santana E, Simões N (2015) New records of ‘opisthobranchs’ (Gastropoda: Heterobranchia) from Arrecife Alacranes National Park, Yucatan, Mexico. Mar Biodivers Rec 8:e117. https://doi.org/10.1017/S1755267215000925
Padula V, Araujo AK, Matthews-Cascon H, Schrödl M (2014) Is the Mediterranean nudibranch Cratena peregrina (Gmelin, 1791) present on the Brazilian coast? Integrative species delimitation and description of Cratena minor n sp J Molluscan Stud 80:575–584. https://doi.org/10.1093/mollus/eyu052
Padula V, Bahia J, Stöger I, Camacho-García Y, Malaquias MAE, Cervera JL, Schrödl M (2016) A test of color-based taxonomy in nudibranchs: molecular phylogeny and species delimitation of the Felimida clenchi (Mollusca: Chromodorididae) species complex. Mol Phylogenet Evol 103:215–229. https://doi.org/10.1016/j.ympev.2016.07.019
Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572. https://doi.org/10.1146/annurev.es.25.110194.002555
Palumbi SR (1996) Nucleic acids II: the polymerase chain reaction. In: Hillis DM, Moritz C, Mable BK (eds) Molecular systematics. Sinauer and Associates, Massachusetts, USA, pp 205–247
Pante E, Schoelinck C, Puillandre N (2014) From integrative taxonomy to species description: one step beyond. Syst Biol 64:152–160. https://doi.org/10.1093/sysbio/syu083
Péron F, Lesueur CA (1810) Tableau des caractères génériques et spécifiques de toutes les espèces de méduses connues jusqu’à ce jour. Annales Mus Hist Nat 14:325–366
Petit RJ, Excoffier L (2009) Gene flow and species delimitation. Trends Ecol Evol 24:386–393. https://doi.org/10.1016/j.tree.2009.02.011
Pola M, Paz-Sedano S, Macali A, Minchin D, Marchini A, Vitale F, Licchelli C, Crocetta F (2019) What is really out there? Review of the genus Okenia Menke, 1830 (Nudibranchia: Goniodorididae) in the Mediterranean Sea with description of two new species. PLoS One 14:e0215037. https://doi.org/10.1371/journal.pone.0215037
Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609. https://doi.org/10.1080/10635150600852011
Portmann A, Sandmeier E (1960) Dondice banyulensis sp. nov. un Eolidien nouveau de la Méditerranée. Rev Suisse Zool 67:158–168
Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Mol Ecol 21:1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using tracer 1.7. Syst Biol 67:901. https://doi.org/10.1093/sysbio/syy032
Ramon ML, Lobel PS, Sorenson MD (2003) Lack of mitochondrial genetic structure in hamlets (Hypoplectrus spp.): recent speciation or ongoing hybridization? Mol Ecol 12:2975–2980. https://doi.org/10.1046/j.1365-294X.2003.01966.x
Redfern C (2001) Bahamian seashells. A thousand species from Abaco, Bahamas. Bahamianseashells.com Inc, Boca Raton Florida.
Redfern C (2013) Bahamian seashells. 1161 species from Abaco, Bahamas. Bahamianseashells.com Inc, Boca Raton, Florida.
Reid N, Carstens B (2012) Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed yule-coalescent model. BMC Evol Biol 12:196. https://doi.org/10.1186/1471-2148-12-196
Risso A (1826) Histoire Naturelle des Principales productions de l’Europe Mèridionale et Particulièrement de Celles des environs de Nice et des Alpes Maritimes. Volume 5. FG. Levrault, Paris, France.
Rocha LA (2003) Patterns of distribution and processes of speciation in Brazilian reef fishes. J Biogeogr 30:1161–1171. https://doi.org/10.1046/j.1365-2699.2003.00900.x
Rocha LA, Bowen BW (2008) Speciation in coral reef fishes. J Fish Biol 72:1101–1121. https://doi.org/10.1111/j.1095-8649.2007.01770.x
Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc London Ser B 272:573–579. https://doi.org/10.1098/2004.3005
Rogers DW, Chase R (2001) Dart receipt promotes sperm storage in the garden snail Helix aspersa. Behav Ecol Sociobiol 50:122–127. https://doi.org/10.1007/s002650100345
Roxo FF, Ochoa LE, Costa-Silva GJ, Oliveira C (2015) Species delimitation in Neoplecostomus (Siluriformes: Loricariidae) using morphologic and genetic approaches. DNA Barcodes 3:110–117
Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352. https://doi.org/10.1111/j.1461-0248.2004.00715.x
Saad L, Cunha CM, Colpo KD, Valdés Á (2014) It’s not what it looks like: molecular data fails to substantiate morphological differences in two sea hares (Mollusca, Heterobranchia, Aplysiidae) from southern Brazil. Helgol Mar Res 68:523. https://doi.org/10.1007/s10152-014-0408-1
Sales JBDL, Rodrigues-Filho LFDS, Ferreira YDS, Carneiro J, Asp NE, Shaw PW, Haimovici M, Markaida U, Ready J, Schneider H, Sampaio I (2017) Divergence of cryptic species of Doryteuthis plei Blainville, 1823 (Loliginidae, Cephalopoda) in the Western Atlantic Ocean is associated with the formation of the Caribbean Sea. Mol Phylogenet Evol 106:44–54. https://doi.org/10.1016/j.ympev.2016.09.014
Sales L, Migotto AE, Marian JEA (2019) Love will tear us apart: traumatic mating through consumption of body parts in a sea slug. Ecology 100:e02849. https://doi.org/10.1002/ecy.2849
Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RaxML. Org Divers Evol 12:335–337. https://doi.org/10.1007/s13127-011-0056-0
Soong GY, Bonomo LJ, Reimer JD, Gosliner TM (2022) Battle of the bands: systematics and phylogeny of the white Goniobranchus nudibranchs with marginal bands (Nudibranchia, Chromodorididae). Zookeys 1083:169–210. https://doi.org/10.3897/zookeys.1083.72939
Sørensen CG, Rauch C, Pola M, Malaquias MAE (2020) Integrative taxonomy reveals a cryptic species of the nudibranch genus Polycera (Polyceridae) in European waters. J Mar Biol Assoc UK 100:733–752. https://doi.org/10.1017/S0025315420000612
Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 4:vey016. https://doi.org/10.1093/ve/vey016
Sun X, Bedos A, Deharveng L (2018) Unusually low genetic divergence at COI barcode locus between two species of intertidal Thalassaphorura (Collembola: Onychiuridae). PeerJ 6:e5021. https://doi.org/10.7717/peerj.5021
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
Thompson TE (1980) Jamaican opisthobranch molluscs II. J Molluscan Stud 46:74–99. https://doi.org/10.1093/oxfordjournals.mollus.a065525
Valdés Á, Hamann J, Behrens DW, DuPont A (2006) Caribbean Sea slugs: a field guide to the Opisthobranch mollusks from the tropical northwestern Atlantic. Sea Challengers, Washington DC, USA
Valdés Á, Gosliner TM, Ghiselin MT (2010) Opisthobranchs. In: Leonard JL, Córdoba-Aguilar A (eds) Primary sexual characters in animals. Oxford University Press, Oxford, UK, pp 148–172
Valdés Á, Lundsten L, Wilson NG (2018) Five new deep-sea species of nudibranchs (Gastropoda: Heterobranchia: Cladobranchia) from the Northeast Pacific. Zootaxa 4526:401–433. https://doi.org/10.11646/zootaxa.4526.4.1
Wilson NG, Burghardt I (2015) Here be dragons—phylogeography of Pteraeolidia ianthina (Angas, 1864) reveals multiple species of photosynthetic nudibranchs (Aeolidina: Nudibranchia). Zool J Linnean Soc 175:119–133. https://doi.org/10.1111/zoj.12266
Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29:2869–2876. https://doi.org/10.1093/bioinformatics/btt499
Acknowledgements
All material was collected by the authors with permission of the host countries or states. We are deeply grateful to all colleagues and friends who provided their support during the different stages of this research: Karina Moreno, Sandra Muro, Kendall Feliciano, and Carla Stout with their help with lab protocols. Ariane Dimitris, Anne DuPont, Daniela Fernandes, and José Henrique Leal provided material for this study. Ronald Janssen of the Senckenberg Naturmuseum Frankfurt provided access to the type material of Dondice occidentalis. We thank the anonymous reviewers for their constructive criticism and valuable comments that improved the manuscript. We thank to the staff of the Institute for Tropical Ecology and Conservation (ITEC) in Bocas del Toro, Panama, specially to Peter Lahanas, Enrique Dixon, Itzel Dixon, and Janet for their collaboration in the field. Gabriel Jacome provided collaboration with the research permits in Panama. To the members of the Department of Marine Sciences of the University of Puerto Rico at Mayagüez, specially to Wendy Ortiz and members of the Schizas Lab: Jaaziel Garcia-Hernandez, Alex Veglia, and Nikolaos V. Schizas for their support during the field sampling in Puerto Rico.
Funding
KGM was supported by CRUSA Foundation Scholarship to pursue her Master’s degree in California. This work was partially supported by the award from the Unitas Malacologica Graduate student Grant to KGM. VP was supported by a research grant from FAPERJ (Programa de Apoio Emergencial ao Museu Nacional; Processo E-26/200.102/2019), Brazil. The SEM work was conducted at the facilities of the Cal Poly Pomona, with the assistance of Anan Hamdan.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethical approval
No animal testing was performed during this study.
Sampling and field studies
All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the acknowledgements, if applicable. The study is compliant with CBD and Nagoya protocols.
Data availability
The datasets generated during and/or analyzed during the current study are available on the Barcode of Life Data System (BOLD) and GenBank datasets repositories. Other datasets generated during and/or the current study are available from the corresponding author on reasonable request.
Author contribution
All authors contributed to specimen collections and molecular data obtained. KGM and AV conducted specimens’ dissections and recorded SEM micrographs. KGM carried out all molecular analyses. All the authors wrote sections in, edited, and approved the final manuscript.
Additional information
Communicated by K. Kocot
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is registered in ZooBank under https://zoobank.org/1D89FDC6-CB3D-456B-8BD9-D648039492E2
Rights and permissions
About this article
Cite this article
García-Méndez, K., Padula, V. & Valdés, Á. Integrative systematics of the genus Dondice Marcus, 1958 (Gastropoda, Nudibranchia, Myrrhinidae) in the Western Atlantic. Mar. Biodivers. 52, 42 (2022). https://doi.org/10.1007/s12526-022-01273-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12526-022-01273-5