A phylogenetic analysis and systematic revision of the cryptobranch dorids (Mollusca, Nudibranchia, Anthobranchia) Author Valdés, Ángel text Zoological Journal of the Linnean Society 2002 2002-12-31 136 4 535 636 https://academic.oup.com/zoolinnean/article-lookup/doi/10.1046/j.1096-3642.2002.00039.x journal article 5419 10.1046/j.1096-3642.2002.00039.x 8acc9095-eaff-47d7-b3da-91b6c2fb636e 0024-4082 4634200 GENUS DORIS LINNAEUS, 1758 Doris Linnaeus, 1758: 653 . Type species: Doris verrucosa Linnaeus, 1758 , by monotypy. Doridigitata d’Orbigny, 1836 -42 [1839]: 39–40, suppressed by Opinion 1980 ( ICZN, 2001 ). Type species: Doris verrucosa Linnaeus, 1758 , by subsequent designation by J. E. Gray (1847) . Doriopsis Pease, 1860: 32–33 . Type species: Doriopsis granulosa Pease, 1860 , by monotypy, syn. nov. Staurodoris Bergh, 1878a: 578–579 , suppressed by Opinion 1980 ( ICZN, 2001 ). Type species: Doris verrucosa Linnaeus, 1758 , by original designation. Archidoris Bergh, 1878b: 616–617 . Type species: Doris pseudoargus Rapp, 1827 , by subsequent designation by Iredale & O’Donoghue (1923) syn. nov. Anoplodoris Fischer, 1880 -87 [1883]: 521. Type species: Doris pseudoargus Rapp, 1827 , by subsequent designation by Iredale & O’Donoghue (1923) syn. nov. Ctenodoris Eliot, 1907: 338 . Type species: Staurodoris pecten Eliot, 1906 , by subsequent designation by Baba (1937) , syn. nov. Austrodoris Odhner, 1926: 67–68 . Type species: Archidoris rubescens Bergh, 1898 , by original designation, syn. nov. Guyonia Risbec, 1928: 102 . Type species: Guyonia flava Risbec, 1928 , here designated syn. nov. Neodoris Baba, 1938: 13–14 . Type species: Neodoris tricolor Baba, 1938 , by original designation, syn. nov. Siraius Marcus, 1955: 134 . Type species: Siraius ilo Er. Marcus, 1955 , by original designation, syn. nov. Doriorbis Kay & Young, 1969: 177–178 . Type species: Doris immonda Risbec, 1928 , here designated syn. nov. Diagnosis Dorsum covered with simple rounded tubercles, stiffened by integumentary spicules, which do not protrude from the dorsal surface. Head with two lateral prolongations. Anterior border of the foot grooved but not notched. Labial cuticle lacking rodlets. Radula composed of simple, hamate teeth. Outermost teeth may be simple or denticulate. Reproductive system with a tubular, granular and simple prostate. Penis and vagina devoid of hooks. Vestibular or accessory glands absent. Remarks Linnaeus (1758) introduced the genus Doris for Doris verrucosa , with a short and confusing Latin description. It is not clear whether Linnaeus studied specimens himself or whether his description was based on the two pre-Linnaean and nonbinomial bibliographical references cited ( Rumphius, 1705 ; Seba, 1735 ). These two papers describe different animals. ‘Limax marina verrucosa’, described by Rumphius (1705: 38) , could be any shell-less gastropod, but probably a species of Phyllidiidae collected from Ambon , Indonesia . Seba’s (1735 : pl. 61, fig. 5) ‘Mitella verrucosa’ is a nudibranch mollusc very likely identifiable as the Indo-Pacific species Phyllidiella pustulosa ( Cuvier, 1804 ) . However, Doris verrucosa has been identified by most authors as the European species described below, characterized by having hemispherical tubercles on the dorsum and numerous unipinnate branchial leaves. The name Doris has also been applied to the relatives of this species, first to all dorid nudibranchs having a circlet of dorsal respiratory leaves, and more recently to just a few species closely related to the mentioned European species. Bouchet & Valdés (2000) submitted a proposal to the ICZN in order to maintain the current usage of the generic and specific names Doris verrucosa by the designation of a neotype . This proposal was endorsed by the ruling of the Commission in Opinion 1980 ( ICZN, 2001 ). D’Orbigny (1836–1842) [1839] segregated Doris into several discrete species groups, which he treated as subgenera. For the new species Doris bertheloti , from the Canary Islands , he established Doridigitata , where he also allocated Doris verrucosa (applying this name to the species mentioned above). Gray (1847) validly fixed Doris verrucosa as the type species of Doridigitata . The genus Doridigitata d’Orbigny, 1839 is an objective junior synonym of Doris because they are based on the same type species. Bergh (1878a) recognized that the original description of Doris did not fit with the usage of the name by most of the authors, and considered that Doridigitata was the valid name for this genus. At the same time, Bergh (1878a) introduced the new name Staurodoris to replace Doridigitata , which according to him was improperly formed. Therefore, Staurodoris and Doridigitata have the same type species and are objective synonyms. Bergh (1878b) introduced the genus Archidoris based on Cuvier’s (1804) misapplication of the name Doris tuberculata Müller, 1778 (see also remarks on Doris pseudoargus ), Doris flammea Alder & Hancock, 1844 and Doris montereyensis Cooper, 1862 . At the same time he mentioned: ‘The spawn and a fragment of the ontogeny of the type of this form [ Archidoris ] is known (see Alder & Hancock)’. Iredale & O’Donoghue (1923) interpreted this comment to mean that Bergh (1878b) had selected a misapplication of the name Doris tuberculata by Alder & Hancock to be the type species of Archidoris . Actually, Bergh’s (1878b) comment cannot be interpreted as the designation of a type species (see ICZN, 1999 : Article 68.2). Therefore, Iredale & O’Donoghue (1923) were the first authors to designate a type species for the genus Archidoris , by subsequent designation. It is clear from the list of species and synonyms included in Archidoris that these authors meant to select the misapplication of the name Doris tuberculata by most authors (= Doris pseudoargus Rapp, 1827 ; see below) as the type species. Thus, according to Article 69.2.4 ( ICZN, 1999 ), Iredale & O’Donoghue (1923) are deemed to have selected Doris pseudoargus Rapp, 1827 as the type species of Archidoris . Examination of the external morphology and anatomy of Doris pseudoargus shows that this species is very similar to Doris verrucosa , with the exception of the presence of large and rounded dorsal tubercles, unipinnate branchial leaves and pectinate outermost teeth in the latter. The phylogenetic analysis carried out (see below) showed that they are members of the same clade. There are no consistent differences that justify the maintenance of two different genera for these closely related taxa. Fischer (1880–1887) [1883] introduced the new genus Anoplodoris Fischer, 1883 to accommodate several nominal genera (and species) previously described. One of these species was cited as ‘ Doris tuberculata Linné’, which constitutes an incorrect citation rather than a misapplication. The name Doris tuberculata was never mentioned by Linnaeus in any of his works. Iredale & O’Donoghue (1923) subsequently designated ‘ Doris tuberculata Linné’ as the type species of Anoplodoris . Again, it is clear that these authors were referring to the misapplication of the name Doris tuberculata by most authors (= Doris pseudoargus Rapp, 1827 ; see below), and by the provisions of Article 69.2.4 ( ICZN, 1999 ), Iredale & O’Donoghue (1923) are deemed to have selected Doris pseudoargus Rapp, 1827 as the type species of Anoplodoris . Because Anoplodoris and Archidoris are based on the same type species they are objective synonyms. Odhner (1926) described the genus Austrodoris based on Archidoris rubescens Bergh, 1898 . According to this author, Austrodoris differs from Doris and Archidoris by having short, wide nonattached salivary glands. In the following years, there was a great deal of confusion between the name Archidoris and Austrodoris , but in general (with a few exceptions) the former was used for species from the northern hemisphere and the latter for species from the southern hemisphere, regardless of the anatomical features of the animals described. Wägele (1990) redescribed the genus Austrodoris and concluded that all species previously described are synonyms of Austrodoris kerguelenensis ( Bergh, 1884 ) . She also maintained the usage of the genus Austrodoris , which differs from Archidoris by having most of the deferent duct covered with a muscular sheath, lacking a glans penis and having the seminal receptacle and the bursa copulatrix inserting opposite and not serially on the vaginal duct. The examination of the type species of the genera Doris and Archidoris has revealed that they also have these features. Thus, there are no consistent differences between these taxa that justify the maintenance of different genus names. Baba (1938) described the genus Neodoris based on Neodoris tricolor Baba, 1938 , the type species by original designation, as different from Doris , Archidoris and Anisodoris . According to Baba (1938) the main distinctive feature of this genus is the absence of a glans penis. He considered Neodoris to be closely related to Austrodoris and Archidoris , but distinguishable by having a prostate gland and band-like salivary glands. Later, Baba (1998) recognized that Neodoris is a synonym of Archidoris , and suggested that Austrodoris could be a synonym as well. Marcus (1955) described the genus Siraius for Siraius ilo Er. Marcus, 1955 from Brazil . He characterized this new genus by the presence of hook-shaped lateral and pectinate marginal teeth, short and grooved oral tentacles, short and wide salivary glands, tubular prostate and penis unarmed. Kay & Young (1969) introduced the genus Doriorbis for a misidentification of Doris nucleola Pease, 1860 (see remarks on Doris immonda Risbec, 1928 ). They characterized this new genus as having simply pinnate branchial leaves arranged as a circlet about a posterior anus, hamate radular teeth with the outermost laterals denticulate, and a Y- or T-shaped medial streak extending from the rhinophores to the middorsum. According to Article 70.3 ( ICZN, 1999 ) if the type species of a nominal genus is found to be misidentified an author may select and fix as the type species the species that will, in his or her judgement, best serve stability. In this case the selection of Doris immonda as the type species clearly serves stability better, as Doris nucleola in the sense of its original description ( Pease, 1860 ) is an unidentifiable species, which has well-developed oral tentacles and probably belongs to a different genus. Brodie & Willan (1993) redescribed Doris immonda (as Doris nucleola ) and considered that it belongs to the genus Siraius Er. Marcus, 1955 . Therefore Doriorbis became a synonym of Siraius . At the same time, they distinguished Siraius from other cryptobranch dorids on the basis of two synapomorphies, the presence of papillae of unequal size around the rhinophoral sheaths, and pectinate outermost lateral teeth. The first character does not have, in my opinion, much phylogenetic significance, and the second is also present in other species of Doris , such as D. pseudoargus . Brodie & Willan (1993) considered Siraius to be closely related to Etidoris Ihering, 1886 ; which is a synonym of Thordisa Bergh, 1877 (see below). Baba (1998) regarded Siraius as a different genus on the basis of the presence of pectinate outermost teeth. The genus Doriopsis was introduced by Pease (1860) based on Doriopsis granulosa . Pease (1860) justified the creation of a new genus on the basis of the arrangement of the gill, which has the leaves ‘disposed in the form of a semicircle, on the posterior portion of the back, and retractile into a similarly formed slit, the convex portion posteriorly’. Four years later, Alder & Hancock (1864) introduced the new genus Doridopsis , which has the same features as Dendrodoris Ehrenberg, 1831 (see Valdés et al ., 1996 ), and only one letter difference from the name Doriopsis Pease, 1860 . Later, Pease (1871a) reaffirmed his genus name Doriopsis as valid and different from Doridopsis . He also argued that Doridopsis should be considered invalid, to avoid confusion with Doriopsis , and erected the replacement name Hanstellodoris Pease, 1871 for it. However, Bergh (1876) regarded Doriopsis and Doridopsis as synonyms, not in the meaning of Pease (1860) but in the meaning of Alder & Hancock (1864) , and accepted Doriopsis as the valid name of the genus. This opinion was accepted by most authors in the following years, and Doriopsis was regarded as a junior synonym and a member of the Porostomata (radulaless dorids). O’Donoghue (1924) considered that Ehrenberg’s name Dendrodoris was valid, and treated Doriopsis and Doridopsis as junior synonyms of the former. Pruvot-Fol (1931) suggested for the first time since Pease (1860 , 1871a ) that Doriopsis is not a synonym of Dendrodoris , but a distinct genus that should be place in the family Archidorididae . On the other hand, Doridopsis is currently regarded as a synonym of Dendrodoris ( Valdés et al ., 1996 ) . Probably unaware of Pease’s (1860) work, Eliot (1907) described the new subgenus Ctenodoris Eliot, 1907 to include Staurodoris pecten Eliot 1906 and Doris flabellifera Cheesman, 1881 . Baba (1937) subsequently selected Staurodoris pecten Eliot, 1906 to be the type species. According to Eliot (1907) the main distinctive feature of Ctenodoris is the structure of the gill, which has the leaves ‘arranged in a line of crescent, and the upper lip of the pocket shuts down over them like a single valve’. This description is very similar to that of Doriopsis , and these two names are clearly synonyms. The genus Guyonia was described by Risbec (1928) on the basis of Guyonia flava Risbec, 1928 , Doris pecten Collingwood, 1881 and Doriopsis viridis Pease, 1861 . Guyonia flava is here designated as the type species. Risbec (1928) described Guyonia as having the general shape of a Platydoris , with small papillae on the dorsum. Radula with unicuspid teeth and penis unarmed. Gill formed of pinnate leaves inserted anteriorly to the anus and forming an convex arch that is retractile under a semicircular lamellae. This description fits with the characteristics of Doriopsis . Baba & Hamatani (1961) regarded Ctenodoris and Guyonia as synonyms of Doriopsis for the first time. The phylogenetic analysis carried out in this paper clearly shows that Doriopsis is a derived member of the clade containing the members of the genus Doris . If Doriopsis is maintained as a separate genus, Doris becomes paraphyletic. The same would probably occur for the rest of the synonyms of Doris if more species were included in the analysis.