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A Synoptic Review of the Family Dendronotidae (Mollusca: Nudibranchia): a Multilevel Organismal Diversity Approach

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A Synoptic Review of the Family Dendronotidae (Mollusca: Nudibranchia): a Multilevel Organismal Diversity Approach ¾ ¿ÀÁ ( ) - CTOZ A synoptic review of the family Dendronotidae (Mollusca: Nudibranchia): a multilevel organismal diversity approach Tatiana Korshunova Koltzov Institute of Developmental Biology, Vavilova str. 26, 119334 Moscow, Russia Torkild Bakken NTNU University Museum, Norwegian University of Science and Technology, Trondheim, Norway Viktor V. Grøtan Ørland Froskemannsklubb (Ørland Diveclub), Postboks 197, 7129 Brekstad, Norway Kjetil B. Johnson Ørland Froskemannsklubb (Ørland Diveclub), Postboks 197, 7129 Brekstad, Norway Kennet Lundin Gothenburg Natural History Museum, Box 7283, 40235, Gothenburg, Sweden Gothenburg Global Biodiversity Centre, Box 461, 40530, Gothenburg, Sweden Alexander Martynov Zoological Museum of the Moscow State University, Bolshaya Nikitskaya Str. 6 125009 Moscow, Russia [email protected] Abstract A synoptic review of the family Dendronotidae is presented based on morphological and molecular data. Three genera are recognized: Dendronotus, Pseudobornella, and Cabangus gen. nov. Two new Dendronotus species are described, D. yrjargul sp. nov. and D. nordenskioeldi sp. nov., which reveal º»ne-scale di¼ferences. Dendronotus yrjargul sp. nov. from mid-Norway and the Arctic regions is a sister species to the North Paciº»c D. kalikal. These two species are showing clear morphological and ontogenetic di¼ferences but are close in genetic distance. In contrast, Dendronotus nordenskioeldi sp. nov. from the Laptev Sea is externally similar to the white morphs of D. lacteus or D. frondosus, but according to the molecular data and radular © ., | : ./- This is an open access article distributed under the terms of the 4.0 license. $ # $# !"%% ./- | . morphology it is distinct from any of its congenerics. Comparison of molecular and morphological data of D. niveus from the type locality (White Sea) and material from other localities with those from the American North Atlantic coast (type locality of D. elegans) reveals their substantial similarity. Therefore, D. niveus is considered a junior synonym of D. elegans. The present review of the family Dendronotidae contributes to a general discussion on the species concepts and on a recent proposal of multilevel organismal diversity. Keywords Cabangus – Dendronotus – Pseudobornella – molecular phylogeny – species problem – taxonomy Zoobank: http://urn:lsid:zoobank.org:pub:5E6F2529-E533-4A89-9EE4-5677865C5468 Introduction criterion of reproductive isolation (Mayr, 1969, 1982) is not robust as has been shown The evolutionary process is traditionally con- on numerous occasions (e.g., McDonald and sidered to be continuous (Darwin, 1859) and Koehn, 1988; Mallet, 2005; Kijewski et al., 2006; this concept prevails despite many years of Harrison & Larson, 2014; Jančúchová-Lásková controversial discussions (Eldredge & Gould, et al., 2015; Crossman et al., 2016; Fraïsse et al., 1972; Mayr, 1982; Mallet et al., 2009; Coates et 2016; Potkamp & Fransen, 2019). al., 2018). However, the species itself is sup- With the dawn of the molecular era in posed to be an unavoidably separate unit taxonomy, the problem of hidden diversity according to the nomenclature of current tax- emerged when molecularly divergent groups onomic practice, which in zoology is governed of specimens were discovered within mor- by the ICZN (1999). This is one of the greatest phologically highly similar species as deº»ned contradictions between the evolutionary pro- in the traditional way (Bickford, 2007; cesses and taxonomic classiº»cation, which Korshunova et al., 2017a, 2019a). The discord- has not been solved satisfactorily (Zachos, ant development of morphological structures 2018). In many cases it has been shown that and genetic apparatus per se is also a sign of it is very di¼º»cult to assign a particular spec- evolutionary processes in progress. However, imen to a particular species. Until now there it is still possible to separate such cases by are no unequivocal and universal criteria for using molecular data and if there are exten- species delimitations when the underlying sive genetic di¼ferences, we may assume that evolutionary processes and phylogenies are evolutionary divergence has occurred among taken into consideration (e.g., Zachos et al., such species. Relatively rarerely noticed and 2013; González et al., 2018; Stanton et al., 2019; much more interesting are those cases when Platania et al., 2020), and even for the exist- despite relatively low genetic di¼ferences ence of species at all (Ereshefsky, 1998; Willis, some species exhibit distinct morphological 2017; Reydon & Kunz, 2019). At the conceptual features (Mayer & Helversen, 2001; Wiemers level, more than 26 di¼ferent species concepts & Fiedler, 2007). The current practice of have been suggested (Zachos, 2016) but at a deº»ning potential species by using molecu- practical level even the most widely acclaimed lar markers depending on various distances $ # $# !"%% Ø À Ø Á ÚÛ ÚØ | ./- and factors (e.g., Ratnasingham & Hebert, ontogenetic data in the framework of mul- 2013) referred to as “operational taxonomic tilevel organismal diversity (Korshunova et units” (s) does not consistently corre- al., 2019a). We therefore develop a general spond to taxa at the species level. There is taxonomic framework for phylogeny and an unfortunate discordance in how the tax- taxonomy of the family Dendronotidae, onomic practice currently works because it which for the º»rst time presents a synoptic is based on a classiº»cation system consist- review of all currently known species of the ing of rigid names that does not fully reÐÑect genus Dendronotus. Its also conº»rms the information of the underlying evolutionary validity of the genus Pseudobornella Baba, processes. A solution for the species prob- 1932 and supports the proposal of the new lem using the separation between metap- genus Cabangus (see details in Synopsis). opulation lineages potentially without any distinguishing characters (de Queiroz, 2006, 2007) contradicts available biological evi- Materials and methods dence, e.g., that even clones show minor but detectable morphological and epigenetic Collecting data di¼ferences. Therefore, to avoid an artiº»cial Specimens were collected by Viktor V. contrast between “cryptic” and “non-cryp- Grøtan and Kjetil B. Johnson in the vicin- tic” species in a classiº»cation and to encom- ities of Trondheim, Norway (63°41’8.66”N pass various available data, the concept 9°39’58.79” E), and also in the Arctic waters of the multilevel organismal diversity was during vessel expeditions, and for compara- proposed (Korshunova et al., 2019a). In the tive purposes by scuba diving in NE Atlantic, present study we apply this approach to the NW and NE Paciº»c. Specimens studied are nudibranch family Dendronotidae. deposited in the collections at Zoological Currently there is an accelerating dis- Museum, Moscow State University (×ØØ), covery of º»ne-scale species-level diver- and the Norwegian University of Science sity within the genus Dendronotus. In the and Technology, NTNU University Museum last decade, 10 of 12 new Dendronotus spp. (-Ø) (Bakken et al., 2020). were described by our research group using both morphological and molecular data Morphological analysis (Martynov 2015a, 2020a; Ekimova et al. 2015; External and internal morphology was stud- Lundin et al., 2017; Korshunova et al. 2016a, ied under a stereomicroscope using a Nikon b, 2017b, 2019b). In this study, we present a D-810 digital camera and scanning electron modern taxonomic synopsis of the family microscopes. The buccal mass of each spec- Dendronotidae, which together with molec- imen was extracted and processed in 10% ular phylogenetic analyses demonstrates sodium hypochlorite solution to extract the both lower and higher degrees of evolution- radula and the jaws. The jaws of each spe- ary separations as a reliable example of mul- cies were analysed under a stereomicro- tilevel organismal diversity. For instance, scope and then photographed. The jaws and a newly discovered species from Norway radulae were coated, then examined and (Dendronotus yrjargul sp. nov.) already has photographed using a scanning electron developed deº»nite signs of morphological microscope (CamScan, JSM). The reproduc- and molecular divergence. This highlights tive systems were also examined using a the importance of considering broadly stereomicroscope. $ # $# !"%% ./- | . Molecular analysis (Ronquist et al., 2012). Four Markov chains Eleven specimens were sequenced for the were sampled at intervals of 500 generations. mitochondrial genes cytochrome c oxi- Analysis was started with random starting dase subunit I (Û ) and 16S rRNA, and the trees and 5 × 106 generations. Maximum nuclear genes 28S rRNA (C1-C2 domain). Likelihood-based phylogeny inference was Small pieces of tissue were used for performed using RAxML 7.2.8 (Stamatakis extraction with Diatom™ Prep 100 kit by et al., 2008)) with 1000 bootstrap replicates. Isogene Lab, according to the producer’s pro- Final phylogenetic tree images were rendered tocols. Standard ÚÛ ampliº»cation options, in FigTree 1.4.2. Nodes in the phylogenetic and sequence obtainment were applied (for trees with Bayesian posterior values > 0.96% details, see Korshunova et al., 2016a, 2017a). and bootstrap values >90% were considered Û sequences were translated into amino ‘highly’ supported. Nodes with 0.90–0.95% acids to verify coding regions and avoid and 80–89% accordingly were considered errors. All new sequences were deposited in ‘moderately’
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