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. 2023 Jan 7;16(2):428-460.
doi: 10.1111/eva.13468. eCollection 2023 Feb.

Narrowly defined taxa on a global scale: The phylogeny and taxonomy of the genera Catriona and Tenellia (Nudibranchia, Trinchesiidae) favours fine-scale taxonomic differentiation and dissolution of the "lumpers & splitters" dilemma

Tatiana Korshunova  1 , Kennet Lundin  2   3 , Klas Malmberg  3   4 , Alexander Martynov  5
Affiliations

Narrowly defined taxa on a global scale: The phylogeny and taxonomy of the genera Catriona and Tenellia (Nudibranchia, Trinchesiidae) favours fine-scale taxonomic differentiation and dissolution of the "lumpers & splitters" dilemma

Tatiana Korshunova et al. Evol Appl. .

Abstract

By applying morphological and molecular data on two genera of the nudibranch molluscs it is shown that the tension between taxonomic practice and evolutionary processes persists. A review of the related genera Catriona and Tenellia is used to demonstrate that the fine-scale taxonomic differentiation is an important tool in the integration of morphological and molecular data. This is highlighted by the hidden species problem and provides strong argument that the genus must be kept as a maximally narrowly-defined entity. Otherwise, we are forced to compare a highly disparate species under the putatively lumped name "Tenellia". We demonstrate this in the present study by applying a suite of delimitation methods and describing a new species of Tenellia from the Baltic Sea. The new species possesses fine-scale morphological distinguishing features, which were not investigated before. The true, narrowly defined genus Tenellia represents a peculiar taxon with a clearly expressed paedomorphic characters and predominantly brackish-water habitats. The phylogenetically related genus Catriona, of which three new species are described here, clearly demonstrates different features. A lumping decision to call many morphologically and evolutionary different taxa as "Tenellia" will downgrade the taxonomic and phylogenetic resolution of the entire family Trinchesiidae to just a single genus. The dissolution of the dilemma of "lumpers & splitters", which still significantly affects taxonomy, will further help to make systematics a true evolutionary discipline.

Keywords: evolution; fine‐scale taxonomic differentiation; molecular phylogeny; mollusca; nudibranchia.

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Conflict of interest statement

We declare that we have no competing interests.

Figures

FIGURE 1
FIGURE 1
Phylogenetic relationships of Catriona and Tenellia based on COI + 16S + H3 concatenated dataset inferred by maximum likelihood (ML). Numbers above branches represent posterior probabilities from Bayesian inference (BI); numbers below branches indicate bootstrap values for ML. Summary of species delimitation results are noted by numbered clusters from the ABGD, ASAP, GMYC and mPTP analyses for the COI and 16S data sets. BS, Black Sea; Sw, Sweden.
FIGURE 2
FIGURE 2
Haplotype network based on cytochrome c oxidase subunit I (COI) molecular data showing genetic mutations occurring within Tenellia gotlandica sp. nov. (red circle) and Tenellia adspersa (blue circles) species.
FIGURE 3
FIGURE 3
Catriona aurantia (Alder & Hancock, 1842). (a) Norway, Gulen, ZMMU Op‐784, ca. 10 mm length (live). (a1) Dorsal view. (a2) Details of ceratal colouration. (a3) Jaws, SEM, 500 μm. (a4) Masticatory edge of jaws with well‐defined bristles, SEM, 10 μm. (a5, a6) Details of bristles, SEM, 10 and 2 μm. (a7) Posterior part of radula, details, SEM, 20 μm. (a8) Posterior part of radula, SEM, 100 μm. (a9) Anterior to middle part of radula, overall view, SEM, 100 μm. (b) Norway, Gulen, ZMMU Op‐545, 4.5 mm length (preserved). (b1) Dorsal view. (b2) Ventral view. (b3) Details of cerata colouration. (b4) Jaws, light microscopy. (b5) Jaw, SEM, 100 μm. (b6) Masticatory edge of jaws, bristles missed, SEM, 5 μm. (b7, b8) Posterior part of radula, details, SEM, 10 μm. (b9) Middle part of radula, details, SEM, 10 μm. (b10) Anterior to middle part of radula, overall view, SEM, 100 μm. (b11) Penis with stylet, SEM 50 μm. (b12) Stylet, details, SEM, 10 μm. Live photos by T. A. Korshunova, A. V. Martynov, SEM micrographs by A. V. Martynov.
FIGURE 4
FIGURE 4
Reproductive systems of Catriona aurantia (Alder & Hancock, 1842) (a), Catriona columbiana (O'Donoghue, 1922) (b), Catriona lucerna sp. nov. (c), Catriona osezakiensis sp. nov. (d), Catriona kishiwadensis sp. nov. (e). Abbreviations: am, ampulla; fgm, female gland mass; fo, female opening; p, penis; pg, supplementary (“penial”) gland; pr, prostate; psh, penial sheath; rs, receptaculum seminis; vd, vas deferens. Scale bars: 500 μm.
FIGURE 5
FIGURE 5
(a–d) Catriona columbiana (O'Donoghue, 1922). (a) USA, Washington state, ZMMU Op‐787, 6 mm length (live). (a1) Dorsal view. (a2) Details of ceratal colouration. (a3) Jaw, SEM, 100 μm. (a4) Masticatory edge of jaws with moderately defined bristles, SEM, 5 μm. (a5) Anterior to middle part of radula, overall view, SEM, 50 μm. (a6, a7) Posterior part of radula, details, SEM, 10 μm. (a8) Preradular long narrow tooth, SEM, 10 μm. (a9) Penis with stylet, SEM, 5 μm. (b) Canada, British Columbia, ZMMU Op‐786, 7 mm length (live). (b1) Dorsal view. (b2) Details of ceratal colouration. (b3) Jaw, light microscopy. (b4) Jaw, SEM, 100 μm. (b5) Masticatory edge of jaws with moderately defined bristles, SEM, 5 μm. (b6, b7) Posterior part of radula, details, SEM, 10 μm. (b8) Middle part of radula, SEM, 10 μm. (b9) Anterior to middle part of radula, overall view, SEM, 100 μm. (c) Russia, the sea of Japan, ZMMU Op‐486, 3.5 mm in length (preserved). (c1) Dorsal view. (c2) Ventral view. (c3) Details of ceratal colouration. (c4) Jaw, light microscopy. (c5) Jaw, SEM, 100 μm. (c6) Masticatory edge of jaws with moderately defined bristles, SEM, 5 μm. (c7) Posterior part of radula, details, SEM, 10 μm. (C8) posterior part of radula, SEM, 20 μm. (c9) Anterior to middle part of radula, overall view, SEM, 100 μm. (c10) Penis with stylet, SEM, 20 μm. (c11) Stylet, details, SEM, 5 μm. (d1) C. columbiana – Neotype, Canada, British Columbia, ZMMU Op‐785, length 8 mm (live). (e1) Catriona spadix (MacFarland, 1966), after original drawing of type specimen, 12.5 mm length (live). (e2) C. Spadix – Radular teeth after original drawing of type specimen in MacFarland (1966). (f1) Catriona alpha (Baba & Hamatani, 1963a), photo of living specimen by Manabu Kakegawa. (f2) C. alpha – Radular teeth after original drawing of type specimen in Baba and Hamatani (1963a). Live photos (if not mentioned otherwise) by T. A. Korshunova, A. V. Martynov, SEM micrographs by A. V. Martynov.
FIGURE 6
FIGURE 6
Catriona kishiwadensis sp. nov. Japan, Osaka region. (a1) Holotype, dorsal view (live), KNHM M10590, ca. 7 mm in length (preserved). (b) KNHM M10590, paratype, ca. 6 mm in length (preserved). (b1) Dorsal view (live). (b2) Ventral view (live). (b3) Jaw, light microscopy. (b4) Jaw, SEM, 300 μm. (b5, b6) Masticatory edge of jaws with moderately to weakly defined bristles, SEM, 10 μm, 30 μm. (b7) Posterior to middle part of radula, SEM, 100 μm. (b8) Anterior to middle part of radula, SEM, 100 μm. (b9) Posterior part of radula, details, SEM, 30 μm. (b10) Middle part of radula, details, SEM, 30 μm. (b11) Anterior part of radula, details, SEM, 10 μm. (b12) Penis with stylet, SEM, 10 μm. Live photos by Sho Kashio, SEM micrographs by A. V. Martynov.
FIGURE 7
FIGURE 7
Catriona lucerna sp. nov. Vietnam, Nha Thrang. (a) Paratype, ZMMU Op‐789, length ca. 7 mm (live). (a1) Dorsal view. (a2) Ventral view. (a3) Details of ceratal colouration. (b) Holotype, ZMMU Op‐788, length ca. 14 mm (live). (b1) Dorsal view. (b2) Ventral view. (b3) Dorso‐lateral view. (b4) Details of ceratal colouration. (b5) Jaw, SEM, 100 μm. (b6) Jaw, light microscopy. (b7) Masticatory edge of jaws with moderately defined bristles, SEM, 10 μm. (b8) Anterior to posterior parts of radula, SEM, 100 μm. (b9) Anterior part of radula, details, SEM, 10 μm. (b10) Middle part of radula, details, SEM, 20 μm. (b11) Posterior part of radula, details, SEM, 10 μm. (b12) Penis with stylet, SEM, 20 μm. (b13) SEM, 5 μm. Live photos by T. A. Korshunova, A. V. Martynov, SEM micrographs by A. V. Martynov.
FIGURE 8
FIGURE 8
Catriona osezakiensis sp. nov., Japan, Osezaki. (a) Holotype ZMMU Op‐790, ca. 12 mm in length. (a1) Dorsal view. (a2) Ventral view. (a3) Details of dorsal colouration. (a4) Jaw, light microscopy. (a5, a6) Masticatory edge of jaws with well‐defined bristles, SEM, 10, 2 μm. (a7) Posterior part of radula, details, SEM, 10 μm. (a8) Anterior to middle part of radula, SEM, 100 μm. (a9) Middle part of radula, details, SEM, 10 μm. (a10, a11) Posterior part of radula, details, SEM, 10 μm. (a12) Penis with stylet, SEM, 20 μm. (a13) Stylet, SEM, 5 μm. (b) Paratype ZMMU Op‐791, ca. 5 mm in length (live). (b1) Dorsal view. (b2) Ventral view. (b3) Details of ceratal colouration. (b4) Jaw, SEM, 100 μm. (b5) Masticatory edge of jaws with well‐defined bristles, SEM, 5 μm. (b6) Posterior to middle part of radula, SEM, 50 μm. (b7) Preradular long narrow teeth, SEM, 10 μm. (b8) Posterior part, details, SEM, 10 μm. (b9) Penis with stylet, SEM, 20 μm. (b10) Penis with stylet, details, 5 μm. (c) Paratype, ZMMU Op‐792, ca. 12 mm in length (live). (c1) Dorsal view. (c2) Ventral view. (c3) Lateral view. (c4) Details of ceratal colouration. (c5) Anterior part of radula, details, SEM, 10 μm. (c6) Posterior part of radula, SEM, 20 μm. (c7) Posterior part of radula, details, SEM, 5 μm. (c8) Jaw, SEM, 50 μm. (c9) Masticatory edge of jaws with weakly defined bristles, 5 μm. (d) Paratype, ZMMU Op‐795, ca. 9 mm in length (live). (d1) Dorsal view. (d2) Ventral view. (d3) Details of ceratal colouration. (d4) Jaw, light microscopy. (d5) Jaw, SEM, 200 μm. (d6) Masticatory edge of jaws with moderately defined bristles, SEM, 20 μm. (d7) Posterior part of radula, SEM, 20 μm. (d8) Middle part of the radula, SEM, 10 μm. (d9) Preradular long narrow teeth, SEM, 10 μm. (d10) Anterior to middle part of radula, SEM, 100 μm. (d11) Penis with stylet, SEM, 10 μm. (e) Paratype, ZMMU Op‐793, ca. 3 mm in length (live). (e1) Dorsal view. (e2) Details of ceratal colouration. (e3) Jaw, SEM, 100 μm. (e4) Masticatory edge of jaws with well‐defined bristles, SEM, 10 μm. (e5) Details of bristles, SEM, 3 μm. (e6) Anterior to middle part of radula, SEM, 30 μm. (e7, e8) Posterior part of radula, SEM, 10 μm, 5 μm. Live photos by T. A. Korshunova, A. V. Martynov, SEM micrographs by A. V. Martynov.
FIGURE 9
FIGURE 9
Tenellia adspersa (Nordmann, 1845). (a) Black Sea, ZMMU Op‐799, length ca. 4 mm (live). (a1) Dorsal view of living specimen in natural environment. (a2) Living specimen, lateral view, light microscopy. (a3) Living specimen, part of dorsal side enlarged, light microscopy. (a4) Jaw, SEM, 50 μm. (a5) Masticatory edge of jaws with irregular denticles, SEM, 20 μm. (a6) Posterior part of radula, 10 μm. (a7) Middle part of radula, SEM, 10 μm. (a8) Anterior part of radula, SEM, 10 μm. (a9) Penis with stylet, SEM, 10 μm. (b) Japan, Osaka region, KSNHM‐M10572, length 2 mm (preserved). (b1) Dorsal view. (b2) Ventral view. (b3) Jaw, SEM, 100 μm. (b4) Masticatory edge of jaws with irregular denticles, SEM, 3 μm. (b5) Posterior part of radula, SEM, 10 μm. (b6) Penis with stylet, SEM, 30 μm. (b7) stylet, details, SEM, 10 μm. (c) The United Kingdom, ZMMU Op‐797, 3–5 mm in length (preserved). (c1) Living specimen, dorsal view (photo by D. Fenwick). (c2) Jaw, SEM, 100 μm. (c3) Masticatory edge of jaws with irregular denticles, SEM, 5 μm, 20 μm. (c4) Posterior part of radula, SEM, 10 μm. (c5) Anterior part of radula, SEM, 10 μm. (c6) Penis with stylet. (d) Baltic Sea, Gotland Island, GNM Gastropoda 9959, 1.5 in length (preserved). (d1) Dorsal view of living specimen (photo by Klas Malmberg). (d2) Jaw, SEM 100 μm. (d3) Masticatory edge of jaws with irregular denticles, SEM, 10 μm. (d4) Anterior part of radula, SEM, 10 μm. (d5) Posterior part of radula, 10 μm. (d6) Penis with stylet, SEM, 20 μm. Live images and photo of preserved specimen (if not mentioned otherwise) by T. A. Korshunova, A. V. Martynov, SEM micrographs by A. V. Martynov.
FIGURE 10
FIGURE 10
Tenellia gotlandica sp. nov. holotype, GNM Gastropoda 9960, length ca. 1.8 mm (preserved), Baltic Sea, Gotland Island. (a1) Dorsal view of living holotype. (a2) ventral view of preserved holotype. (a3) jaw, SEM, 50 μm. (a4) masticatory edge of jaws with irregular denticles, SEM, 5 μm. (a5) posterior part of radular teeth, SEM, 10 μm. (a6) posterior part of radular teeth, details, SEM, 10 μm. (a7) anterior part of radula, SEM, 10 μm. (a8) penis with stylet, SEM, 20 μm. (a9) stylet, details, SEM, 10 μm. Live image by Klas Malmberg, photo of preserved specimen by T. A. Korshunova, A. V. Martynov, SEM micrographs by A. V. Martynov.
FIGURE 11
FIGURE 11
Reproductive systems of Tenellia adspersa (a), Tenellia gotlandica sp. nov. (b). Abbreviations: am, ampulla; fgm, female gland mass; fo, female opening; p, penis; pg, supplementary (“penial”) gland; pr, prostate; psh, penial sheath; rs, receptaculum seminis; vd, vas deferens. Scale bars: 500 μm.
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