Flabellinidae, a family of nudibranchs in controversy

During the year 2017 several articles have been published that propose a series of changes affecting the phylogenies of different families of nudibranchs. Among these articles there are two that significantly affect the Flabellinidae family.

Furfaro et al. (2018, published online September 6th, 2017) have done an interesting job to clarify the status of the Flabellinidae family in the Mediterranean and the real affinities between their species. Using mitochondrial and nuclear sequences both from collected specimens and GenBank sequences, from species of the genera Calmella, Flabellina and Piseinotecus, from the Mediterranean, Eastern and Western Atlantic, Pacific and Antarctica, and studying their radular morphology, they build a phylogenetic tree of the different species and reach the following conclusions:

• The families Flabellinidae and Piseinotecidae are not monophyletic.
• There are two well differentiated clades (groups), that of Coryphella pedata and similar species with cerata growing directly from the back of the animal and that of Flabellina affinis and similar species, with the cerata growing from a stalk or pod growing from the back of the animal, which they consider an important synapomorphy of the clade while the individual union of each cerata to the back is considered a plesiomorphy.
• Genus Calmella is synonymous with Flabellina.
• Species Calmella cavolini, Piseinotecus gaditanus and Piseinotecus gabinierei are included in the genus Flabellina, as F. cavolini, F. gaditana and F. gabinierei respectively. In the case of the two species initially attributed to Piseinoteus, P. gaditanus and P. gabinierei, the authors show that their radulas are triseriate and not monoseriate, which classifies them within the Flabellinidae and not within the Piseinotecidae.
• The species Flabellina confusa of the North-East Atlantic is synonymous with F. gaditana.
• The Atlantic and Mediterranean populations of Flabellina ischitana have sufficient molecular differences (minimum p-distance of 12.5%) to be considered two different species. Admitting the Mediterranean specimens as F. ischitana, the Atlantic ones are possibly a new species still under study.
• Calmella cavolini and Flabellina confusa / Piseinotecus gaditanus species, in addition to having a very similar morphology, have very low genetic distances of 5.0%, which, together with the relatively large intraspecific divergence found in C. cavolini (1.8%), means that a more in-depth study must be conducted to find out if they are two different species or the same species with a big genetic variability.

The goal of Furfaro et al. was to molecularly characterize the Mediterranean species by comparing them with other GenBank data of species from the Atlantic and other geographic areas.

Korshunova et al. (2017) is based on both molecular analysis (COI, 16S, 28S and H3 genes) and morphological analysis of Flabellinidae species from the Arctic, North Atlantic, Pacific and Indian Oceans. This extensive article confirms the polyphily of the Flabellinidae family and represents an authentic revolution not only for the taxonomy of the Flabellinidae but for the organization in families of all the aeolidaceans. The authors also focus on the fact that the phylogeny of the Flabellinidae can not be understood without considering members of other Aeolidacea families and that morphological characters, not only molecular ones, must have their importance when establishing phylogenies. In Figure 2 of their paper they show the resulting phylogenetic tree with the relationships between the different families and genera of the Aeolidacea. Among the many conclusions of this paper the most interesting ones are:

• Three new families are proposed to include species that were within the traditional Flabellinidae: Apataidae, Flabellinopsidae and Samlidae.
• Families Coryphellidae and Paracoryphellidae are restored.
• Unidentidae family is confirmed based on morphological and molecular data.
• The new genera Polaria and Ziminella are created within the Paracoryphellidae family.
• The new Baenopsis genus is created within the Flabellinopsidae family.
• The new genera Borealea, Fjordia, Gulenia, Itaxia, Microchlamylla, Occidenthella and Orienthella are created within the Coryphellidae family.
• The new genera Carronella, Edmundsella and Paraflabellina are created within the Flabellinidae family.
• The new Pacifia genus is created within the Unidentiidae family.
• The new genus Luisella is created within the new Samlidae family.
• The new Apata genus is created within the new Apataidae family.
• The genus Piseinotecus remains within the Flabellinidae family.
• The Calmella genus remains within the Flabellinidae family.

All these changes of new genera and families of the paper by Korshunova et al. affect many European Flabellinidae species, such as:

• Flabellina baetica García-Gómez, 1984 is transferred to the genus Baenopsis as B. baetica (García-Gómez, 1984), within the new Flabellinopsidae family.
• Flabellina verrucosa (M. Sars, 1829) is transferred to the genus Coryphella as C. verrucosa (M. Sars, 1829) within the Coryphellidae family.
• Flabellina browni Picton, 1980 is transferred to the new genus Fjordia as F. browni (Picton, 1980) within the Coryphellidae family.
• Flabellina lineata (Lovén, 1846) is transferred to the new genus Fjordia as F. lineata (Lovén, 1846) within the Coryphellidae family.
• Flabellina insolita García-Gómez & Cervera, 1898 based on morphological traits only is transferred to the new genus Fjordia as F. insolita (García-Gómez & Cervera, 1898) within the Coryphellidae family.
• Flabellina gracilis (Alder & Hancock, 1844) is transferred to the new genus Microchlamylla as M. gracilis (Alder & Hancock, 1844) within the Coryphellidae family.
• Flabellina gaditana (Cervera, García-Gómez & García, 1987) originally described as Piseinotecus gaditanus is transferred to the genus Calmella as C. gaditana (Cervera, García-Gómez & García, 1987) within the Flabellinidae family.
• Flabellina cavolini (Vérany, 1846) is restored to the genus Calmella as C.cavolini (Vérany, 1846) within the Flabellinidae family.
• Flabellina pellucida (Alder & Hancock, 1843) originally described as Eolis pellucida (Alder & Hancock, 1843), is transferred to the new genus Carronella as C. pellucida (Alder & Hancock, 1843).
• Flabellina pedata (Montagu, 1815) originally described as Doris pedata Montagu, 1815 and published by many authors as Coryphella pedata, is transferred to the new genus Edmundsella as E. pedata (Montagu, 1815), within the Flabellinidae family.
• Flabellina ischitana Hirano & Thompson, 1990 is transferred to the new genus Paraflabellina as P. ischitana (Hirano & Thompson, 1990), within the Flabellinidae family.
• Flabellina gabinierei (Vicente, 1975), originally described as Facelina gabinierei Vicente, 1975 and published in many later papers as Piseinotecus gabinierei (Vicente, 1975), is transferred to the new genus Paraflabellina as P. gabinierei (Vicente, 1975), within the Flabellinidae family.
• Flabellina babai Schmekel, 1972 is transferred to the new genus Luisella as L. babai (Schmekel, 1972), within the new family Samlidae.

The paper by Korshunova et al. aims to delve into the phylogenetic relationships between the various members of the Flabellinidae family and the other families of the Aeolidaceans, adding many new species from Northern Europe, the Arctic and the North Pacific.

Similarities and differences

When comparing the results of both articles, although they are very different because the first mainly studies Mediterranean species, while the second focuses on Arctic and North Pacific species, they obtain some very similar results, which can be seen in the following figure, built with the phylogenetic trees proposed by both works (A = Furfaro et al.; B=Korshunova et al.).

For example, both trees show two well-defined main clades, that of Flabellina pedata and “similars”, with cerata growing individually straight from the back of the animal (red circles in the figure) and that of Flabellina affinis and “similars”, with cerata growing in groups, attached to a common stalk or pod (blue circles in the figure).

However, although Furfaro et al. consider the species of both clades belonging to the genus Flabellina within the family Flabellinidae, in Korshunova et al. they dived them in two families Coryphellidae and Flabellinidae sensu stricto, also creating different genera in these families to accomodate the species they study, some of them of Arctic distribution, so within the Flabellina genus they only consider one species, F. affinis.

Furfaro et al. do not provide the genetic distances between the different species of the two main clades but they do indicate the possible existence of a cryptic speciation in the Flabellinidae and recommend additional molecular studies. Interestingly, this is what Korshunova et al. provided, almost in synchrony with the work by Furfaro et al.

Furfaro et al. indicate that Flabellina babai behaves like an unstable taxon (rogue taxon) that appears located in different places of the previous phylogenetic trees; in the tree represented in Figure 1 of their paper this species is shown as an independent branch from the main bifurcation, not being grouped within another upper clade. By eliminating this species from the analysis set to build the phylogenetic tree, the support values ​​of the different nodes increase, something that can be seen in Figure 2 of their paper.

In contrast, in the paper by Korshunova et al. F. babai is included within the family Samlidae as a basal clade to the Aeolidacea. These authors recognize the great morphological differences between the genus Samla and Flabellina babai, so they describe a new genus Luisella, separated from Samla by molecular distances between 19% and 21%, enough to consider both genera valid. However, although we provisionally accept the change of family and genus of Flabellina babai to Luisella babai (Schmekel, 1972) within the new Samlidae family, we believe that more morphological and molecular analysis based on a broader sampling of Flabellina babai throughout the Atlanto-Mediterranean area are necessary to definitively clarify its taxonomic position.

(…) we believe that more morphological and molecular analysis based on a broader sampling of Flabellina babai throughout the Atlanto-Mediterranean area are necessary to definitively clarify its taxonomic position.

The species Flabellina baetica appears differentiated from the two main clades of the Flabellinidae sensu lato, both in the paper by Furfaro et al. and the paper by Korshunova et al.; these last authors create the genus Baenopsis for this species, that together with genus Flabellinopsis form the new family Flabellinopsidae, basal to the traditional Flabellinidae.

Both papers coincide in grouping in the same clade Calmella cavolini / Piseinotecus gaditanus and this as sibling of the clade formed by Flabellina ischitana / Piseinotecus gabinierei.

Furfaro et al. confirm by optical and scanning electron microscopy (SEM) the triseriate radula (although the lateral teeth are rudimentary and smooth) of Calmella cavolini, Piseinotecus gaditanus and Piseinotecus gabinierei and also how these species are found, in the phylogenetic tree, in the same clade as Flabellina affinis, including these three species within the genus Flabellina as F. cavolini, F. gaditana and F. gabinierei (Table 2 of their paper). Also, and due to the small genetic distance between the two species, they synonymize Flabellina confusa with Flabellina gaditana. Furfaro et al. do not indicate the genetic distances between these species compared with F. affinis.

This tendency to group species into the same genus by Furfaro et al. it is opposed to the more extensive work by Korshunova et al., which preserves the genera Flabellina, Calmella, Coryphellina and Piseinotecus (this one with doubts), and also create new genera for other clades that they obtain in their tree for the Flabellinidae sensu stricto. So:

• Create the genus Paraflabellina to include Flabellina ischitana and Piseinotecus gabinierei as Paraflabellina ischitana (Hirano & Thompson, 1990) and Paraflabellina gabinierei (Vicente, 1975), respectively.
• Create the genus Carronella to include Flabellina pellucida, Carronella pellucida (Alder & Hancock, 18432) and the new species Carronella enne from Northeast Ireland.
• Create the genus Edmundsella to include Coryphella pedata and Flabellina albomaculata as Edmundsella pedata (Montagu, 1815) and Edmundsella albomaculata (Pola et al., 2014) respectively.

In Table 2 of their paper, Korshunova et al. (2017) provide the minimum p-distances between the representatives of each of the previous genera, ranging from 13.1% between Edmundsella pedata and Coryphelina rubrolineata and 20.2% between Paraflabellina funeka and Carronella pellucida. As remarkable data, the genetic distances between Calmella cavolini and Flabellina affinis are 17.4% and between Flabellina affinis and Edmundsella pedata are 15.0%. All these genetic distances, so far and until new opinions appear, are enough to consider that they belong to different genera.

Korshunova et al. reinstate the family Paracoryphellidae Miller, 1971 to include the genus Chlamylla Bergh, 1886 with species from the Arctic and the Barents Sea as Chlamylla borealis Bergh, 1886 and the new species Ch. intermedia, and the genus Paracorhyphella Miller, 1971, with a species of northern Europe, Paracoryphella islandica (Odhner, 1937) (originally described as Coryphella islandica) and another new species from the Sea of ​​Japan P. ignicrystalla. They also create the new Polaria genus, with a single Polaria polaris (Volodchenko, 1946) species (originally described as Coryphella polaris) from the Arctic, and Ziminella genus that integrates species from the Arctic, the Sea of ​​Japan and the North American Atlantic coast, as Ziminella salmonacea (Couthouy, 1938) (originally described as Eolis salmonacea), Z. japonica (Volodchenko, 1937) (originally described as Coryphella japonica) and the new species Z. abyssa and Z. circapolaris.

The family Coryphellidae is also reinstated by Korshunova et al. In the tree of this family (Figure 2 of their paper) statistically well defined small clades can be observed; each of the branches of these clades correspond to species of different genera, such as the well-known Coryphella and Himatina, and the new genera Borealea, Gulenia, Fjordia, Itaxia, Microchlamylla, Occidenthella and Orienthella. So:

• The genus Coryphella now only includes two species, C. verrucosa of the North Atlantic and C. pseudoverrucosa of the North Pacific.
• The genus Himatina contains a single species Himatina trophina (Bergh, 1894) (originally described as Himatella trophina) from the North Pacific.
• They create the genus Borealea with two species, B. nobilis (Verrill, 1880) (originally described as Coryphella nobilis) and the new species from the North Pacific B. sanamyanae.
• The new genus Gulenia includes three northern European species, Gulenia borealis (Odhner, 1922) (originally described as Coryphella borealis) and two new species, G. orjani and G. monicae.
• The new genus Fjordia is the most diverse of all the Coryphellidae, with 5 species, among which the European species F. lineata (Lovén, 1846) (Eolis lineata in the original description), F. insolita (García-Gómez & Cervera, 1989) (Flabellina insolita in the original description), F. browni (Picton, 1980) (Coryphella browni in the original description), the new species F. chriskaugei from the coast of Norway and the South African species F. capensis (Thiele, 1925) (originally Coryphella capensis).
• The new genus Itaxia is created with a single species Itaxia falklandica (Eliot, 1907) (original description as Coryphella falklandica) found in the Falkland Islands and southern Chile.
• The new genus Microchlamylla is created with two species, Microchlamylla gracilis (Alder & Hancock, 1844) (originally described as Eolis gracilis) from northern Europe and M. amabilis (Hirano & Kuzirian, 1991) (originally Flabellina amabilis).
• The new genus Occidenthella with a single species Occidenthella athadona (Bergh, 1875) (original description as Corhyphella athadona) of the western Pacific.
• The new genus Orienthella, with the Pacific species Orienthella trilineata (O’Donoghue, 1921) (originally described as Coryphella trilineata), Orienthella fogata (Millen & Hermosillo, 2007) (originally described as Flabellina fogata) and Orienthella cooperi (Cockerell, 1901 ) (originally described as Coryphella cooperi).

The minimum molecular differences (p-distances) between the representatives of all these genera of Coryphellidae vary from 10.1% between Fjordia chiskaugei and Himatina trophina to 18.3% between Orienthella trilineata and Itaxia falklandica (Table 1 of the paper by Korshunova et al.).

All the changes proposed by Korshunova et al. seem to be accepted by WoRMS database as of December 31, 2017.

Conclusions

When there are not fully concordant data between similar papers as those discussed above, we have the dilemma of assessing the results in the most objective way to take the most appropriate position.

The proposal to create new genera to join small groups of species, rather than multispecific genera, seems to be the trend in some of the recent phylogenetic papers. (…) It is possible that more works will follow this trend from now on, with the inconvenience of the early expiration of part of the phylogenetic information contained in the articles when other more recent results are published. A possible solution to this problem would be a greater intercommunication between the different research groups to join efforts and thus obtain phylogenetic trees with greater solvency and widespread acceptance.

It is evident that the work by Korshunova et al. deals with a much larger group of species (126 specimens) than that by Furfaro et al. (23 species); also that the main objective of Furfaro et al. was to molecularly characterize the Mediterranean species by comparing them with other GenBank data of species from the Atlantic and other geographic areas, while the work by Korshunova et al. wanted to delve into the phylogenetic relationships between various members of the Flabellinidae family and the other families of the Aeolidacea, adding many new species from Northern Europe, the Arctic and the North Pacific.

The proposal to create new genera to join small groups of species, rather than multispecific genera, seems to be the trend in some of the recent phylogenetic papers. For an example in this line, in addition to the aforementioned article by Korshunova et al., in Zamora-Silva & Malaquias (2017) they perform the molecular phylogeny of the Aglajidae family (Heterobranchia, Cephalaspidea) based on 412 collected specimens that generated 345 molecular sequences and using 490 other GenBank sequences conclude the existence of 63 species within the family, belonging to 15 different generic lineages, of which seven are described as new genera: Biuve, Camachoaglaja, Mannesia, Mariaglaja, Niparaya, Spinophallus and Tubulophilinosis.

It is possible that more works that follow this trend from now on, with the inconvenience of the early expiration of part of the phylogenetic information contained in the articles when other more recent results are published. A possible solution to this problem would be a greater intercommunication between the different research groups to join efforts and thus obtain phylogenetic trees with greater solvency and widespread acceptance.

Although the work by Korshunova et al. has a solid base of morphological and molecular information of the studied species, we miss a greater sampling of tropical flabellinid species from the Indopacific and the Atlantic, as well as species fron the colder coasts of South America and southern Africa.

The phylogenetic analysis in the Heterobranchs (formerly Opisthobranchs) are “in full boil”, works on phylogenies of small or large taxa constantly appearing, and even proposing that the appearance of evolutionary lineages may have been a consequence of the dietary specialization of their members (Goodheart et al., 2017).

At OPK, we accept -with some caution- the changes proposed by Korshunova et al. in their work reviewing the Flabellinidae while there is no other more recent information that modifies them.

Bibliography