Comment on Fehér et al. (2013): Molecular phylogeny of Alopia

Hartmut Nordsieck (VIII.2013)


The paper of Fehér et al. (2013) succeeds in showing that oppositely coiled (= enantiomorph) species of Alopia are real species and dextrality has originated more than once, but fails in reconstructing the phylogeny within the genus and proposing a revised system, mainly by non-consideration of the interspecific hybridization which is proved to occur in the genus.

In the following, the page numbers of the citations from the commented paper are given in brackets.
The names of Alopia species taxa are used without consideration of their taxonomic rank (for further information see Nordsieck 2008).


1. Enantiomorph taxa are species, not subspecies:

„... the presence of more than one abundant species in the Piatra Craiului (A. glorifica and A. lischkeana), Bucegi (A. livida and A. monacha (= straminicollis)), and Ciucas (Alopia canescens and Alopia nefasta) ranges. These examples show that although infraspecific differentiation was usually confined to a particular mountain, co-occurrence in the same mountain does not necessarily mean close phylogenetic relationship” (268).
This means that the enantiomorph species of Alopia are actually species, not subspecies (in contrast to the former papers of Szekeres, e. g. 1976). Strange to say that the work of Grossu & Tesio (1972) using allozymes for the differentiation of the enantiomorph taxa which had clearly the same result is completely ignored.

2. Dextral taxa have originated polyphyletically:

„The COI-based phylogram implies that the dextral taxa did not evolve as a monophyletic lineage that stemmed from an inversion early in Alopia phylogeny. Instead, they appeared polyphyletically as the results of several independent inversions, rendering dextral coiling a homoplastic trait in this genus” (266-267).
Dextral taxa of Alopia are no monopyletic group but have originated more than once.

3. Relationships of far distant subspecies are confirmed:

„The molecular data also revealed hitherto unrecognized phylogenetic relationships between Alopia forms separated by large geographical distances” (267).
The close relationships of similar, but far distant taxa (which, however, were not unrecognized, Nordsieck 2008) are confirmed, and further ones have been discovered:
A. clathrata belonging to A. bielzii;
A. julii belonging to A. livida;
. vranceana belonging to A. glorifica;
A. microstoma = A. petrensis and A. nordsiecki belonging to A. regalis;
A. peregrina = A. monacha;
A. soosiana = A. pomatias.

4. Taxonomic changes are postulated:

„... indicates that the subspecies formerly belonging to A. plumbea (bellicosa and plumbea in clade B2) and those of A. regalis (deubeli, glabriuscula, mutabilis, proclivis, regalis, and wagneri in clade C1) represent two distinct evolutionary lineages” (267).
This means that A. plumbea and A. regalis should be regarded as independent species.


1. COI-tree is incomplete:

In the COI-tree published in the paper the branch support values are not given, but some, not all, in Appendix S2, which is only online available.
Weak points of the COI-tree are: „... the topology of the major clades had relatively weak support in the COI phylogram” (268), and „... failed to identify a consistent root position relative to the out-groups” (265).
Root positions are not given in the paper, but in Appendix S3, thus only online available. Two are preferential, one in group A and one in group C. It is difficult to understand why plesiomorphic character states of shell and genital morphology of Alopia (Nordsieck 2008) are not considered to discuss the root positions.

2. Morphological characters are insufficiently considered:

„We propose a taxonomic division which is compatible with molecular and morphological characters“ (261), and: „Tree topologies in taxonomically unambiguous groups (e.g. clades A and F) were in full agreement with the morphology-based classification; therefore, we assumed similar good agreement between the COI phylogeny and speciation in groups with less distinctive morphological features. Accordingly, the taxonomic division we propose is based on the evaluation of both molecular data and morphological characters” (267).
However, all information on shell and genital morphology of Alopia species given in the text is the following: „... the rugose shell wall of A. bielzii, the characteristic lump behind the peristome of A. bogatensis, or the elongated male genital structures of Alopia glauca, Alopia maciana and Alopia pomatias” (267).
In Appendix S5, only online available, further information on morphological characters is given. It is restricted to the coiling direction, the sculpture, the clausilium and the length of the male copulatory organs; other informative characters, like shell colour, further characters of the clausilial apparatus and further characters of the genitalia, are not considered. Besides, the traits are given for the species of the new system; those of several taxa now regarded as infraspecific remain unclear.
Thus, the morphological characters are insufficiently considered; the proposed system is nearly exclusively based on the COI analysis.

3. Interspecific hybridization is not considered:

„These data indicate close evolutionary relationships within these taxon pairs of opposite chirality but otherwise identical morphology (Fig. 3)” (266).
The close relationships can also be caused by interspecific hybridization. If mtDNA is used for phylogenetic purposes it must be excluded that interspecific hybridization has occured. This hybridization, however, is a frequent phenomenon within the genus Alopia (Szekeres 1976, Nordsieck 1979, 2007, chapter VI).
In the following species pairs of the COI-tree with syntopic or close parapatric occurrences hybridization can have influenced the tree topology (in brackets possible gene flow):
A. intercedens A. deceptans (= A. lischkeana) (identical haplotypes!) (A. glorificaA. lischkeana);
A. boettgeriA. cybaea (= A. obesa) (A. lischkeana A. glorifica);
A. mariaeA. hildegardae (A. hildegardaeA. subcosticollis);
A. mauritiiA. helenae (A. helenaeA. canescens);
A. nixaA. fussi (A. nixaA. fussi or A. fussiA. nixa, respectively);
A. occulta A. fortunata (A. subcosticollisA. hildegardae).
In the following species pairs obviously not, though hybridization has been demonstrated:
A. straminicollisA. livida;
A. galbinaA. livida;
A. nixaA. livida.
To the species pair of the Piatra Craiului Mountains the following is said: “The relationship between A. glorifica and A. lischkeana, both native to the Piatra Craiului Mountains, requires better insight. Although COI sequences suggest only a distant relationship between these species, their morphological similarity raises the question whether indeed they are of distinct origin“ (268).
In the paper different results of COI sequence comparison of A. glorifica and A. lischkeana are given:
The sequences of these species are
1. very divergent (in other parts of the mountains, where they occur allopatrically),
2. very similar (A. boettgeri and A. cybaea = A. obesa in Valea Râului, where they occur syntopically), or
3. identical (A. intercedens and A. deceptans = A. lischkeana in Cheile Seacă, where they also occur syntopically).
All forms of A. glorifica and of A. lischkeana, respectively, are connected by intermediates so that they cannot be affiliated with different species, as is proposed in the new system.

4. Proposed system is insufficiently founded:

„... based on our results we make taxonomic statements when this is essential for the consistency of the classification that we use” (265).
In the paper (e. g., in table 1) a new system based on COI analysis is used, without foundation (e. g., how the species are delimited).
To the subgenus A. (Kimakowiczia) the following is said: „the subgeneric separation of this group is not supported by the COI phylogeny, which shows the same depth of divergence for the Alopia (Kimakowiczia) group as for the other major clades of the genus (Fig. 2)” (268).
High divergence of genital characters, on which the subgenus is based, must not be found again in the divergence of the COI sequences of the group (= F). Because: „Genetic drift effects may be behind the apparent discrepancy between the more diverse morphological traits in Alopia and the less diverse indispensable COI genes” (269).

5. Taxa are not adequately treated:

1. Contrary to „... these taxon pairs of opposite chirality but otherwise identical morphology” (266), A. nixa and A. fussi are morphologically not identical but different in genital morphology (Szekeres 1976, Grossu 1981). The difference is so clear that it induced Szekeres to create for the first species the new subgenus A. (Nixa). Now, in the new system, A. nixa belongs to the same species as A. fussi.

2. The description of the new taxon A. deceptans by Deli & Szekeres (2011) is a remarkable case of COI based taxonomy overturning morphologically based taxonomy, without considering all possibilities. This taxon, which I could also collect in Cheile Seacă together with A. glorifica, can morphologically not be distinguished from A. lischkeana. Its COI sequence, which according to the commented paper is identical with that of A. glorifica occuring syntopically, could be caused by a shift of mitochondria from A. glorifica to A. lischkeana by interspecific hybridization (see 3.).

3. A. alpina is in shell morphology nearly indistinguishable from A. glorifica. In the commented paper it is treated as an independent species, without further discussion.

4. A. straminicollis and A. monacha are so similar in shell morphology (they have therefore been confused by several authors, Nordsieck 1979) that they cannot be separated as independent species as proposed in the commented paper, without further discussion.

5. A. bogatensis „B” (= A. laevigata, name preoccupied, Nordsieck 2008) and A. bogatensis „A” (= A. bogatensis) are obviously so divergent in COI sequence that they should be separated as subspecies. Strange to say that this is not proposed in the new system of the commented paper.

6. Determined divergence age is improbable:

„... estimated the divergence of the major Alopia clades at 1.2 Mya, with a 95% highest posterior density interval of 1.6–0.8 Myr“ (265), and: „placing this event at the middle of the Pleistocene, appears to be a realistic estimate” (268). Another age from mtDNA: „... the roughly 10.4 Mya calculated with the canonical ~1% rate used previously for mitochondrial DNA sequences” (268), is refused.
A divergence age of 1.2 my for the genus Alopia is quite improbable. On the other hand, an age of 10.4 my is convenient to the stem age leading to Alopia given in Uit de Weerd & Gittenberger (2013: 209, tree).
Other arguments for a higher divergence age are the following:
A species of the genus Triloba (Alopiinae), which is as divergent from extant species of that genus as the Alopia species from one another, is of Late Miocene age (Schnabel 2012).
Species of genera of other subfamilies (e. g., Clausiliinae) which exhibit a similar divergence as Alopia species have Pliocene age (Nordsieck 1990).
„The modest (13.0%) intrageneric pairwise divergence of COI sequences in Alopia, as compared with those of the Balkan genera Albinaria (18.2%), Carinigera (19.9%) and Inchoatia (17.8%), also implies that this is a relatively young genus in the Alopiinae” (268).
But, like Albinaria and other genera, it has probably not originated in the Pleistocene. According to Uit de Weerd & Gittenberger (2013: 209, tree) only few closely related genera of Clausiliidae have separated in the Pliocene (e. g., Lampedusa and Muticaria, Siciliaria and Papillifera), no one in the Pleistocene. Genera of the Alopiinae from southeastern Europe have separated not later than those of the other subfamilies from remaining Europe.
The clausiliid faunas of the Early and Middle Pleistocene of western and central Europe are similar to the Recent one; radiations of clausiliid groups could not be traced during that period (Nordsieck 2007, chapter XI and website art. 2013). It is improbable that this was much different for faunas of southeastern Europe.
As to the separation of dextral species from sinistral ones: „The dextral lineages of A. bielzii (clade A1) and A. meschendorferi (clade E) show deep divergence (Fig. 2), whereas some others reveal only minor or no changes of the COI sequence relative to the closest related sinistral taxa“ (267).
This means that the separation of dextral lineages happened at different times, some relatively early.


Deli, T. & Szekeres, M. (2011): Two new dextral subspecies of Alopia H. & A. Adams 1855 (Gastropoda: Clausiliidae). – Malakológiai Tájékoztató [Malacological Newsletter], 29: 19-23.

Fehér, Z., Németh, L., Nicoară, A. & Szekeres, M. (2013): Molecular phylogeny of the land snail genus Alopia (Gastropoda: Clausiliidae) reveals multiple inversions of chirality. – Zool. J. Linn. Soc., 167: 259-272.

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Nordsieck, H. (2013): Plio-pleistozäne Clausiliidae (Gastropoda, Stylommatophora) von Mitteleuropa nördlich der Alpen, mit besonderer Berücksichtigung der Clausilienfauna von Deutsch-Altenburg 4B (Niederösterreich). –

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