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Taxon sampling, character sampling and
systematics: how gradist presuppositions
created additional ganglia in gastropod
euthyneuran taxa
BENOIT DAYRAT* AND SIMON TILLIER
Muskurn national d’tiistoire naturelle, Institut de Systimatique (WRS FR 1541), Luboratoire
de Biologie des InvertLbrLs marins et de Malacologie (CNRSESA 8044), 55, rue Bufon, F75005 Paris and Service de Systhatigue moliculaire, 43, rue Cuuier, F-7500.5 Paris, France
Received March 1998, accepted for publication 3anuary 1999
In gastropods, the pentaganglionate condition of the nervous visceral loop has been accepted
as a general character and one of the most important synapomorphies of the Euthyneura.
The review of published data on 50 generic ta?ta shows an extreme confusion in both
terminology and application of the homology concept to the two parietal ganglia obsened
in some Euthyneura, in addition to the three obsewed in most gastropods. A parsimonious
re-interpretation of the data leads to the conclusion that the occurrence of five visceral
ganglia is ascertained in only six genus-group taxa, and therefore cannot be accepted as a
general character of Euthyneura. We propose that in phylogrnetic analysis, taxonomic
sampling should be determined according to the variability of characters and independently
of the rank of the taxa taken into account, until every taxon in the data matrix is monomorphic
for every character, and until all the taxa in which the characters occur are represented in
the data matrix. We propose to use the term ‘domain of definition’ of a character for such
a taxonomic sample. Implementing the domain of definition of characters in construction of
data matrices would avoid the abuse of generalities leading to circularity in evolutionary
interpretations of classification, which in the case of Euthyneura result from an a priori gradist
interpretation of the evolution of the nervous system.
0 2000 The Linnean Society of London
ADDITIONAL KEY WORDS:-Mollusca
Gastropoda
polymorphism - homology - central nervous system.
~
~
Euthyneura
-
phylogeny
CONTENTS
Introduction . . . . . . . . . . . . . . . . . .
The central nervous system of gastropods . . . . . . .
Interrelationship of taxonomic sampling and character sampling
Anatomy and terminology . . . . . . . . . . . .
Homology of parietal ganglia . . . . . . . . . . .
Interpretation of complex and various topologies . . .
A heterogeneous terminology . . . . . . . . . .
* Corresponding author.
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E-mail: [email protected]
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0 2000 The Linnean Society of London
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R. DPIYRAT AND S. TILLIEK
Fusion of ganglia . . . . . . . . . . . . . . . . . . . . .
Serial sections and relative size . . . . . . . . . . . . . .
Innervation . . . . . . . . . . . . . . . . . . . . .
DeveloDmental studies . . . . . . . . . . . . . . . . .
Irnniunocytocheniical studies . . . . . . . . . . . . . . .
Range of the pentaganglionate condition in euthyneuran gastropods . . .
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Criteria . . . . . . . . . . . . . . . . . . . . .
Range of the pentaganglionate condition in Pentaganglionata . . . .
Domain of definition of the character ‘triganglionate/pentaganglionate’ .
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Conclusion . . . . . . . . . . . . . . . . . . . . .
Acknowledgements
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References . . . . . . . . . . . . . . . . . . . . .
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INTRODUCIION
The use, and the risk of abuse, of generalization is an old problem in natural
sciences (e.g. Tournefort, 1700, pop popd from the Latin by Becker, 1954: 295).
Anatomical descriptions did not escape the practice of generalization. Most often
characters observed in one or very few subtaxa are considered general and characteristic of the whole taxon which includes those subtaxa, and many diagnostic
descriptions of taxa in all famous handbooks of zoology and botany include such
terms as ‘generally, mainly, many, in majority, most o f . .... Necessarily, with the
use of generalization comes the concept of exception. These presuppositions on
which is the general character and which is the exception were never rejected-or
even discussed-in gradistic systematics, because of the perfect agreement with one
of the principles of the latter, following which general equals primitive and exceptional
equals advanced.
In phylogenetic systematics a ‘generality’ and its correlated ‘exceptions’ must be
rejected as such, and the corresponding character states must be tested in terms of
plesiomorphy and apomorphy by parsimony analysis. Only the latter permits
inference of the history of a character from the phylogenetic pattern. In cladistics
the ‘generality’ does not exist prior to cladistic analysis because the concept can be
relevant only after monophyletic taxa have been defined. After cladistic analysis, it
is not more useful because either the character occurs in all members of the taxon,
or in only some of them but its occurrence in the common ancestor of the taxon is
inferred from the analysis. In both cases, the unambiguous term and concept applied
to such a character is symplesiomorphy; there is no need in cladistic classification
for distinction between general and exceptional, which is a statistic and not a
phylogenetic concept. Phylogenetic systematics allows discussion of the evolutionary
history and significance of each character (Hennig, 1966; Mayr, 1969: 86; Wiley,
198l), which is fundamental because characters do not evolve altogether, but rather
exhibit mosaic evolution (heterobathmy of characters: Takhtajan, 1959). A priori
acceptance of gradistic generalities implies that the history of characters cannot be
traced or discussed because the taxa and their characters are predetermined: the
use of generalities transforms the methodology of phylogenetic systematics into
confirmation of preceding gradistic assertions.
Generalization, as used here, consists in supposing the occurrence of character
states in taxa, although this occurrence has not been supported by any observations.
It is different from commonality, as used in methodological works concerning
polymorphism, which results from description and allows distinction of statistically
common states from statistically exceptional states (Arnold, 198 1).
SAMPLING IN SYSTEPIMTICS
405
In the present paper we discuss the triganglionate/pentaganglionate condition of
the visceral loop because of its importance in the phylogeny and classification of
Gastropoda, and because it provides a good example of what we think is abuse of
a gradistic generality in phylogenetics. The analysis of this character leads us to a
strict definition of an operational concept in systematics: the domain of definition
of a character.
THE CENTRAL NERL’OUS S\-STEhl OF GASTROPODS
The nervous system of gastropods has provided important characters for classification since the beginning of the last century (Hoffmann, 1939; Haszprunar, 1988;
Ponder & Lindberg, 1997).It comprises (Fretter & Graham, 1994, fig. 23; Haszprunar
& Huber, 1990, fig. 3) an anterior circumoesophageal nerve ring and a posterior
visceral loop originating from two ganglia of the ring. The circumoesophageal nerve
ring includes two cerebral, two pleural and two pedal ganglia, and the visceral loop
joins the two pleural ganglia and includes from none to six ganglia. This visceral
loop is highly variable among gastropods in both length and organization. In 1881,
Spengel introduced the major distinction between the streptoneuran (twisted) or
euthyneuran (not twisted) condition of the visceral loop upon which he subdivided
Gastropoda Cuvier, 1798 into two subclasses, Streptoneura and Euthyneura. From
the observation that the long streptoneuran visceral loops never include more than
three ganglia, Plate (1895) interpreted a left additional ganglion, which he named
parietal, as a neoformation in Euthyneura. He produced an evolutionary tree of the
euthyneuran gastropods in which Actaeon is the ancestor of pulmonates and tectibranchs, the tectibranchs being the ancestors of the nudibranchs. The occurrence
of two left and right parietal ganglia in the visceral loop was discussed by various
authors (Minichev, 1967; Brace, 1983) and was emphasized by Haszprunar (1985,
1988)as “one of the most important synapomorphous character” for the euthyneuran
gastropods, because “these parietal ganglia occur in all Pentaganglionata”. Consequently, Haszprunar introduced the name Pentaganglionata as a synonym of
Euthyneura. Although Bieler (1 990) noted critically that according to Haszprunar’s
‘clado-evolutionary’ conception of phylogenetics, this synapomorphy was not tested
by any parsimony procedure, the synapomorphous pentaganglionate condition and
Pentaganglionata has been widely accepted by malacologists-without any discussion
by Salvini-Plawen and Steiner (1996), and after a short discussion by Ponder and
Lindberg (1997).
T o explain variability in the number of ganglia of the visceral loop of the
‘Pentaganglionata’, which cannot be totally ignored, Haszprunar (1985) asserted
that the “parietal ganglia occur in all Pentaganglionata during embryogenesis, but
are variably fused with other ganglia”, and cited four papers supporting this
statement (Hoffmann, 1939; Riedl, 1960; RCgondaud, 1974; Brace, 1977). Although
Haszprunar and Huber again asserted in 1990 that “it is possible to start each
concentration-line with a basal condition characterized by five ganglia at the visceral
loop”, the homology of the ganglia of the visceral loop remains a question (Ponder
& Lindberg, 1997). Actually, the visceral loop of adult Euthyneura includes from
none to six ganglia. The hypothesis of repeated ontogenetic fusion is an ad hoc
generalization, which should be tested by phylogenetic analysis. However, before
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B. DAYRAT AND S. TILLIER
the latter is possible, the available data on ontogenesis and anatomy of the nervous
system of gastropods have to be carefully re-evaluated in terms of both primary
homology and corresponding terminology,
INTERRELATIONSHIP OF TAXONOMIC SAMPLING AND CHARACTER SAMPLING
Because a tree topology reflects data which are analysed in a definite data set,
the constitution of the latter and the related construction of a matrix are the most
important steps in a phylogenetic analysis (e.g. Pogue & Mickevich, 1990). The
construction of the data matrix involves three major interrelated steps: (1) definition
of a monophyletic group including the taxa under study; (2) definition of characters
upon which homology is hypothetized a priori in this group, and which exhibit more
than one state within the group; (3) analysis and coding of character states in each
taxon of the group. The last step often shows that some of the taxa admitted a priori
are not homogeneous for some character states. For such taxa, such characters are
usually either coded as polymorphic, or are oriented a priori in order to code only
the presupposed plesiomorphic state in the taxon under consideration, or are coded
as missing data (Smith, 1994). Surprisingly, taxa sampling is not revised even though
in such cases the distribution of character sites objectively challenges the monophyly
of these taxa. Logically, the data matrix should be constituted by taxa which are
homogeneous for every of their character states, which implies that a priori accepted
polymorphic taxa should be split into subtaxa until all taxa in the matrix are
monomorphic for each character (this is what Mayr (1969), although not a supporter
of phylogenetic systematics, already asserted in an intraspecific context).
In our opinion, the sampling of characters and their variability are interlinked
with taxonomic sampling, and both should be determined jointly before any
phylogenetic reconstruction. It has already been shown that taxa sampling directly
influences the topology of the trees (Lecointre, 1993; Sanderson, 1996).Polymorphism
has already been discussed in a phylogenetic context, but with the objective to code
polymorphism as a single character state, i.e. accepting the monophyly of the
polymorphic taxa (see e.g. Mabee & Humphries (1993) and Rannala (1995) who
discussed the use of allozyme polymorphism at intraspecific level). However, while
these and other authors have discussed either polymorphism or taxa sampling, it
seems that none has formally established their linkage.
The consequence of our statement is that the taxonomic sample used in the data
matrix should be determined in accordance with the variation of each character
submitted to analysis. We call the taxonomic sample so constituted the ‘domain of
definition’ of a character. This domain is defined independently for each character,
and the taxonomic sample used for a given set of characters is therefore the
combination of the domains of definition of all characters used, where every a priori
accepted (primary) taxon is subdivided as far as necessary into subtaxa until every
(secondary) taxon in the matrix is monomorphic for every character state. In
molecular phylogeny the problem of the domain of definition does not exist because
of the methods and techniques used: single and therefore monomorphic organisms
are used; only variable characters (sites) of which states are objectively defined are
taken into account; and generalization of observed character states to taxa is done
only a posteriori, after tree construction. In morphology, the definition of character
SAMPLING IN SYSTEMATICS
40 7
states and related taxonomic sample is obviously more complex, and may result in
involuntarily overweighting a priori hypotheses which cannot be tested by the
subsequent procedure.
In any monophyletic taxon each character has only one domain of definition.
The domain of definition is independent of the rank of the taxa. As an example,
let us suppose a character with two states 0/1; five taxa A, B, C, D and E; and
their subtaxa ( a , . . . a ; . . .a,,), (b, . . . b;.. . blo),(c, . . . c i . . . cIo),(d, . . . d i . . . d,,) and
( e l . . . e i . . . elo).The character exhibits the state 0 in A, B, C, (dl, dp, d3)and (el, e2,
e3)and the state 1 in the others (d, . . . dlo)and (e4.. . el,). The domain of definition
ofthis character is {A, B, C, (d, . . . d; . . . dlo),(el . . . ei . . . e,,)}. Even if the monophyly
of A, B, C, D, and E has been demonstrated formerly, D and E must be split in
the matrix because: (1) this split may influence the interrelationships of A, B, C, D,
and E; and (2) it is necessary to analyse the history of characters. A taxon which is
recognized as a unit in the domain of definition of a character can be divided into
elementary subtaxa according to the domain of definition of other characters. In
our example, let us suppose a second character of which the domain of definition
is {(a, . . . a;. . . a,,), B, C, D, E}. In the data matrix taking both characters into
account, the domain of definition is { ( a , . .. a i . . . a,,), B, C, (dl. . . d;. . . dlo),
(el . . . ei . . . elo)}.The domain of definition is therefore unique for each character
and for each set of characters taken independently, but varies as a function of the
characters taken into account: addition or subtraction of characters influences the
definition of the domain of definition in a given monophyletic group.
Splitting the taxa under study may be insufficient to constitute the domain of
definition of a character: enlarging the set of taxa until all taxa in which the character
occurs are represented may also be necessary. Phylogenetic analysis is possible only
(1) when the ingroup is monophyletic, and (2) when all the taxa which exhibit a
character state found in the ingroup are present, whatever their rank, in the data
matrix, even though many of them do not belong a priori to the ingroup. Let us
suppose that A, B, C, D and E constitute an ingroup, and that another taxon, F, is
not included a priori in the data matrix. Let us further suppose that a character
which occurs in A, B, C, D, E and F varies within the latter. The subtaxa of F must
be added to the domain of definition of this character, and thus in the set of taxa
of the data matrix. Synapomorphy can be tested only if the set of taxa where each
character state occurs is complete. Exclusion of taxa which exhibit character states
observed in the ingroup from the matrix may be an operational necessity, but
implies acceptance of homoplasy between these taxa and the ingroup for these
character states, and should be justified.
The relationship between the homology of a character and its domain of definition
is then obvious: the former does not depend on character states and their distribution
within the group under study, whereas the latter, which varies as a function of these
parameters, is the application of the hypothesis of homology to data set construction
for phylogenetic analysis.
ANATOMY AND TERMINOLOGY
In the caenogastropod Littorina littorea (Linnaeus, 1758) the circumoesophageal
nerve ring includes three pairs of ganglia (Fretter & Graham, 1962): two dorsal
408
B. DAYRAT AND S. TILLIER
cerebral, two lateral pleural and two ventral pedal ganglia. The cerebral and pedal
ganglia are joined respectively by the transversal cerebral and pedal commissures.
Three connectives join respectively the pleural and pedal, the pedal and cerebral,
and the cerebral and pleural ganglia on each side. A long visceral loop joins the
left and right pleural ganglia and innervates the visceral mass. In Littorina littorea, the
visceral loop includes only one left suboesophageal, one abdominal and one right
supraoesophageal ganglia and is then called triganglionate (Fretter & Graham, 1994,
fig. 23). In Acteon tornatilis (Linnaeus, 1758) which belongs to the Euthyneura sensu
Spengel and Boettger, and to the Pentaganglionata sensu Haszprunar, the visceral
loop is as long as in Littorina but includes two more ganglia, and is then called
pentaganglionate (Hoffmann, 1939, fig. 476; Haszprunar & Huber, 1990, fig. 3):
one ‘left parietal’ between the left pleural and the suboesophageal and one ‘right
parietal’ between the right pleural and the supraoesophageal (Bouvier, 1893; Guiart,
1901; Hoffmann, 1939; Brace, 1983).
The abdominal ganglion of gastropods is called ‘visceral ganglion’ by many
authors. In order to avoid confusion, we use here the term ‘visceral ganglia’ to
designate all the ganglia of the visceral loop, and the term ‘abdominal ganglion’ for
the unpaired posterior ganglion of the visceral loop. To describe the anatomical
composition of the visceral loop in a simple way, we use the diagram proposed by
Mikkelsen (1996), slightly modified. { P1-PaSb-(AbSp)-Pa-Pl} is the formula for
a pentaganglionate visceral loop with left parietal, suboesophageal, abdominal,
supraoesophageal, right parietal and two pleural ganglia. {. . .} denotes the limits
of the visceral chain, pleural ganglia included. Hyphens indicate occurrence of a
visible connective, and brackets indicate apparent fusion of ganglia. The diagram
above therefore indicates: (1) that the left parietal ganglion is close to the suboesophageal one, but without a distinct connective; (2) that the abdominal is fused
with the supraoesophageal; and (3) that the right parietal is joined to the right
pleural by a distinct connective.
HOMOLOGY OF PARIEI’AL GANGLIA
Interpretation
of complex and various topologies
In Gastropoda the visceral loop exhibits various anatomical aspects and arrangements, and exhibits from none to five visceral nervous masses, each nervous
mass including one or more ganglia. These visceral nervous masses have been
diversely interpreted. Although the pentaganglionate condition has been considered
‘primitive’ in Euthyneura (Bargmann, 1930; Hoffmann, 1939; Haszprunar, 1988),
many hypotheses of fusion have been proposed to explain the various topologies
(Wirz, 1952).
(1) Many authors did not mention or describe any fusion implying parietal ganglia
but some others, from similar observations of the same objects, mentioned fused
parietal ganglia because of the presupposed ‘primitive’ pentaganglionate condition,
without any new information. For example, in Gastropteron, Hoffmann (1939) added
a left parietal ganglion which was absent in Vayssikre’s (1880) description; in Hydatina,
Ringicula and Cylichna, Mikkelsen (1 996) added parietal ganglia which were absent
in Lemche’s (1956) and Rudman’s (1972a) descriptions.
SAMPLING IN SYSTEMATICS
409
(2) In contrast to pseudo-observations of such ‘virtual’ parietal ganglia, parietal
ganglia have never been mentioned in the visceral loop of many taxa, like Oxynoe
(Burn, 1966; Jensen, 1980) and in Thecosomata (Pelseneer, 1880; Meisenheimer,
1905; Hoffmann, 1939).
(3) Fusions which had been hypothetically proposed by an author have been used
as actual observations by others: in Scaphander, according to Guiart (190 1) and Brace
(1977), the left parietal ganglion is “probablement” and “supposedly” fused to the
corresponding pleural while according to Mikkelsen (1996), the same ganglion is
“considered fused with the pleural by Brace (1977) and Schmekel(1985)”(Schmekel’s
statement is based upon citation of Guiart’s paper). Thus, a fusion which has never
been more than hypothetized becomes taken as granted with time and may be
finally accepted without any new data.
(4) In nudibranchs, developmental data are inconsistent. Baba (1937), Thompson
(1958, ) and Bickell & Chia (1979) did not describe any appearance of a visceral
loop and ganglia in the development of Okadaih, Doridella, Adalaria and T ~ t o n i a
respectively. However, in Aeolidiella, Tardy (1 974) described the primary appearance
of a pentaganglionate visceral loop and the secondary fusion of the visceral ganglia
with the cerebro-pleural ganglia.
A heterogeneous terminology
As noted by Basch (1959) concerning Pulmonata, the heterogeneity of the
terminology used for visceral ganglia of the euthyneuran gastropods by various
authors precludes coherent hypotheses on their homology. For example:
(1) Kerkut and Walker (1975) used two different terminologies in the same paper
for Chilina and Lyrnnaea.
(2) In 1945 and 1975, Hubendick gave different and incompatible interpretations
of the visceral ganglia of Amphibola-{ Pa-(SbAb)-Pa} in 1945 and { Sb-Ab-Sp} in
1975.
(3) In Chilina, Harry (1964) mentioned one left parietal ganglion and one right
parietal ganglion because of their parietal position, but stated explicitly their
homology with the suboesophageal and supraoesophageal ganglia of prosobranchs.
In all gastropods, Naef (19 1 1) and Merker (19 13) have called the suboesophageal
and supraoesophageal ganglia respectively ‘left parietal’ and ‘right parietal’. For
them, the visceral loop of Lyrnnaea would have been { PlPa( = Sb)AbPa(= Sp)Pl}.
(4) In stylommatophoran pulmonates, the visceral loop exhibits three or less
nervous masses in all taxa in which this character has been observed (Tillier, 1989).
Within the loop the central mass has been called ‘visceral ganglion’ ( = abdominal),
and the two lateral ganglia have been called ‘parietal’ without any reference to
homology or non-homology with supra- and suboesophageal ganglia.
(5) In the streptoneuran, triganglionate Marisa (Ampullarioidea) Demian & Youssif
(1975) qualify the same ganglia either ‘intestinal’ ( = sub- and supraoesophageal), or
‘parietal’ because of their parietal position. So many other examples can be found
that it is impossible to determine without complete revision, for any term used,
whether an hypothesis of homology is implied when a given term is used.
Nevertheless, many authors proposed terminologies in relation to theories based
on processes supposedly involved in evolution of euthyneury.
410
B. DAYRAT AND S. TILLIER
(1) According to Pelseneer (1901), euthyneury implies fusion between the suboesophageal ganglion and the abdominal one, and the ganglion located between
the abdominal and the left pleural is a neoformation, i.e. the left parietal ganglion:
“le correspondant gauche (chez les dextres) du ganglion supra-intestinal, n’est pas
homologue de l’infra-intestinal des Streptoneura: c’est une formation nouvelle, le
ganglion pariktal”. Pelseneer (1901: 46) described this new left and additional
parietal ganglion in Acteon, Akera and in Pulmonata, and he described only one
supraoesophageal ganglion on the right side. According to Pelseneer, the visceral
loop of Lymnaea would be { PlPa(SbAb)SpPl}.
(2) Bargmann (1930) considered that the pentaganglionate condition is ‘primitive’
in Euthyneura and introduced many new hypothetical fusions to explain the
pattern of the visceral loop. Her interpretation of the visceral loop of Lymnaea is
{ PlPa(SbAb)(SpPa)Pl}.
(3) Krull’s ‘zygosis theory’ (1933) involved (a) appearance of two new left and
two new right parietal ganglia, (b) fusion between the suboesophageal and the
abdominal and finally, (c) loss of the supraoesophageal. One of the strong arguments
against this theory is that it implies that the osphradium of streptoneurans is not
homologous with the one of the Euthyneura (because it is not innervated from the
same ganglion). According to Krull, the visceral loop of Lymnaea is { Pa(SbAb)Pa}.
(4) Hubendick (1945) proposed a new ‘zygosis theory’, but later (1978) simply
used the terminology ‘suboesophageal’ and ‘supraoesophageal’. His interpretation
of the visceral loop of Lymnaea is { SbAbSp}.
One can easily conclude that homologies of visceral ganglia have not only never
been determined with certainty, but have even been subject of contradictory
hypotheses. In such conditions, one can hardly determine when homology is intended
by authors.
FUSION OF GANGLIA
Whereas the fusion of cerebral and pleural ganglia of the nerve ring is evidenced
by double lateral connectives, corresponding respectively to the cerebro-pedal and
pleuro-pedal, there is no such simple criterion supporting hypothetical fusions
of visceral ganglia which are central in phylogenetic hypotheses in Euthyneura
(Haszprunar & Huber, 1990). However, hypotheses on fusions of ganglia do not
rely only on such projections as shown above, and anatomical observations have
been used to support some of them.
Serial sections and relative size
Serial sections have been invoked as a criterion for fusion in visceral ganglia, the
idea being probably that separating walls, or their remnants, should be observed
when a single mass results from fusion of two ganglia (e.g. Ghiselin, 1963). From
published observations, it does not seem that anyone ever observed such separation
in serial sections of putatively fused ganglia (Hubendick, 1945, in Amphibola;
Meisenheimer, 1905 and Hoffmann, 1939 in the thecosome Hyalocylix). Even in
their exemplary work on the visceral loop of Smeagol based upon serial sections,
SAMPLING IN SYSTEMATICS
41 I
Haszprunar & Huber (1990) describe ganglia fused { (P1Pa)-(SbAb)(SpPa)Pl}
because
of their relative size, but do not mention any microscopical trace of separation
(according to them, the left parietal is fused with the left pleural because the left
pleural is bigger than the right pleural ganglia). The same remark applies to Huber’s
work on the cerebral nervous system of marine Heterobranchia (1993: 394), in
which some visceral loops are described, and in which only relative size, and
seemingly no microscopical observations, is used to assert fusions of ganglia (e.g.
Philinoglossa).Therefore it seems that relative size, which actually may be determined
more precisely from serial sections, is the criterion used to hypothetize fusions of
ganglia. This may be an indication, but it is not conclusive because obviously many
assymmetries in ganglion size are not the result of fusions.
Innmation
The innervation of homologous organs has been used as a criterion for homology
of the ganglia from which the corresponding nerves originate in the central nervous
system (e.g. the osphradial nerve allows identification of the supraoesophageal
ganglion in different visceral loops of Apogastropoda: Haszprunar, 1988). However,
such specific innervation has not been found for the nerves issued from the parietal
ganglia. These nerves may be either mentioned as present or absent in a single
taxon (Brace, 1983; Guiart, 1901; Huber, 1993; Mikkelsen, 1996; Pelseneer, 1901);
or even seemingly totally absent in other taxa (Hubendick, 1978; Huber, 1993;
Lacaze-Duthiers, 1872; Lemche, 1956; Pelseneer, 1901). This confusion causes
contradictory interpretations: for example, Dieuzeide (1935) and Marcus & Marcus
(1960), in Siphonaria, described similar innervations from the ganglia of the visceral
loop, but proposed two different hypotheses of fusion of these ganglia. Whereas
there is no specific and unambiguous nerve originating from parietal ganglia, some
authors have used the occurrence of a nerve originating from the visceral loop as a
trace of a parietal ganglion where this ganglion is anatomically absent (Guiart, 1901;
Mikkelsen, 1996; Schumann, 191 1).
Developmental studies
While discussing the appearance of the parietal ganglia in ontogeny, Ponder &
Lindberg (1997) noted that they have never been mentioned in the development of
many species. Many authors indeed described only a triganglionate loop in many
euthyneuran gastropods: in Adalaria and Tritonia (Thompson, 1958, 1962), Retusa
(Smith, 1967), Limax (Henchman, 1890), Planorbis, Lymnaea and Physa (Fol, 1879),
Achatina (Ghose, 1962),Apbsia (Kriegstein, 1977), and Ovatella (Ruthensteiner, 1991).
Baba (1937), Bickell & Chia (1979) and Thompson (1958, 1962) have respectively
described in Okadaza, Domiella, Adalaria and Tiitonia (nudibranchs) the direct development of the nervous system without any appearance of visceral loop. In Melibe,
Page (1992)described the fusion of “cerebral, subintestinal and visceral ( = abdominal)
ganglia on the left side and cerebral, supraintestinal, and possibly parietal and
osphradial ganglia on the right side”. Only Riedl (1961) in Rhodope, Tardy (1974)
in Aeolidiella and Rtgondaud (1961, 1964 and 1974) in Lymnaea, have mentioned the
occurrence of a pentaganglionate visceral loop during development. Developmental
412
B. UAYRAT AND S. TILLIER
studies are therefore inconsistent regarding plesiomorphy of the pentaganglionate
condition. The embryology of Acteon could be critical to understanding the origin
and development of parietal ganglia, because its visceral loop is unambiguously
pentaganglionate when adult.
Immunoytochemical studies
The localization of the expression of neuronal peptides could provide a criterion
of homology of ganglia. For example, in Aphsia californicu Weiss et al. (1989)
characterized a gene coding for three neuronal peptides ( R 1 5 ~ 1R15P,
,
and R15y)
which is expressed in the R15 neuron, originating from the abdominal ganglion
(Kandel, 1979). Recently, Kerkhoven et al. (1991) showed the expression of a gene
highly similar to the latter (VD1-RPD2) in the central nervous system of bmnaea
stagnalis. This gene is expressed in the VD1 and RPD2 neurons, which originate
from the abdominal ganglion and from the right parietal ganglion respectively, but
is expressed also in neurons originating from cerebral and pedal ganglia. It is
therefore not possible to deduce presently any homology in visceral ganglia from
these data because the expressions of R15 and VD1-RPD2 are not specific to any
ganglion in the central nervous system, but such studies could provide useful data
from other genes.
RANGE OF THE PENTAGANGLIONATE CONDITION IN EUTHYNEURAN GASTROPODS
Criteria
Further to the above discussion, we propose the following criteria to interpret the
composition of the visceral loop when at least three nervous masses may be observed:
(1) The left and right ganglia must be described separately, because many visceral
loops are not symmetrical and are tetraganglionate (with the right but no left parietal
ganglion) like Cylichna.
(2) When five ganglia can be distinguished in the visceral loop, the condition is
pentaganglionate.
(3) The fusions implying parietal ganglia as defined here, and which are not
demonstrated, are not accepted and the simpler interpretation of the observed
topology is always retained for the adult visceral loops. When only three visceral
ganglia can be distinguished in the visceral loop, the condition of the latter is
interpreted as triganglionate until a different condition is demonstrated.
(4)If the data are inconsistent or if the character pentaganglionate/triganglionate
has been the object of incompatible descriptions within a genus-level taxon, the
loop is called ‘problematic’.
We do not consider visceral loops including only one or two nervous masses in
the visceral mass, nor those taxa in which the visceral loop is absent, because these
are not informative for assessing the homology of the parietal ganglia. The former
states occur in many gastropod subtaxa otherwise tri- or pentaganglionate, and the
latter is found, as stated above, in some nudibranchs.
SAMPLING IN SYSTEMATICS
413
Range of the pentaganglionate condition among Pentaganglionata
Pentaganglionate loops. Acteon (Guiart, 190 1); Aeolidiella (Tardy, 1974); Akera (Guiart,
1901); Cylindrobulla (Marcus & Marcus, 1956); Lutia (Pelseneer, 1901); Rhodope (Riedl,
1960).
Ztraganglionate loops. Cylichna (Lemche, 1956); Scaphander (Guiart, 1901).
Tiganglionate loops. Aglaja (Gosliner, 1980); Amphibola (Hubendick, 1945); Apbsia
(Kriegstein, 1977); Archidois (Hoffmann, 1939); Arion (Van Mol, 1962); Berthella
(Hoffmann, 1939); Clione (Meisenheimer, 1905); Colpodaspis (Brown, 1979); Diaphana
(Hoffmann, 1939); Ellobium (Marcus & Marcus, 1965); Ebsia (Russell, 1929);
Gastropteron (Gosliner, 1989); Helix (Kerkut & Walker, 1975); Henaea (Gascoigne,
1979); Hydromyles (Meisenheimer, 1905); Limacina (Hoffmann, 1939); Limupontia
(Jensen, 1993); Melanochlamys (Rudman, 1972b); Otina (Pelseneer, 1901); Ovutella
(Ruthensteiner, 1991); Oxynoe (Jensen, 1980); Peraclis (Meisenheimer, 1905); Phyllapbsia (Marcus & Marcus, 1957); Planorbis (Fol, 1879; Lacaze-Duthiers, 1872);
Ringicula (Fretter, 1960); Siphopteron (Gosliner, 1989); Smaragdinella (Rudman, 1972d);
Titonia (Hoffmann, 1939); Glodina (Vayssihre, 1883); Umbraculum (Moquin-Tandon,
1870); numerous stylommatophoran genera (Tillier, 1989).
Problematic loops. Bulla (Hoffmann, 1939; Brace, 1977); Chilina (1894, 1901; Harry,
1964; Hubendick, 1978; Brace, 1983; Ituarte, 1997); Haminoea (Rudman, 1971;
Mikkelsen, 1996); Hydutina (Eales, 1938; Rudman, 1972a; Mikkelsen, 1996); Lymnaea
(Fol, 1879; Mac Craw, 1957; Rtgondaud, 1974); Melibe (Page, 1992); Onchidella
(Joyeux-Laffiuie, 1882; Van Mol, 1967); Philine (Brown, 1934; Rudman, 1972c;
Mikkelsen, 1996);Retusa (Smith, 1967; Mikkelsen, 1996); Siphonaiu (Dieuzeide, 1935;
Marcus & Marcus, 1960; Hubendick, 1978); Eronicella (Hoffmann, 1925; Coiffmann,
1934; Van Mol, 1967); Voluatella (Burn, 1966;Jensen & Wells, 1990).
Domain of definition
of the character
‘triganglionate/pentaganglionate’
According to Haszprunar (1988) and Salvini-Plawen & Steiner (1996), a pentaganglionate visceral loop occurs in all Euthyneura and is absent in all the supposedly
monophyletic streptoneuran taxa. Then, according to these authors, the domain of
definition of the character (triganglionate/pentaganglionate) is: { streptoneuran taxa;
Euthyneura}. From the distribution of the pentaganglionate state in the list given
above, the non-stylommatophoran Euthyneura must be divided into subtaxa of
generic rank. The suprafamilial or familial streptoneuran taxa, which do not
constitute a monophyletic taxon, should not be pooled in spite of their homogeneous
condition (plesiomorphic), because the monophyly of the euthyneuran taxa is not
demonstrated, and the sister taxon of the latter is not identified. In conclusion, the
domain of definition is {supposedly monophyletic subtaxa of Streptoneura; taxa of
generic rank of non-stylommatophoran Euthyneura; Stylommatophora}.
Contrary to Salvini-Plawen & Steiner (1996), Ponder & Lindberg (1997) discussed
the variation of the pentaganglionate state in the Euthyneura but using four subtaxa
only: Acteonidae, Chilinidae, Amphibolidae and Aplysiidae. The interpretation
which results from their phylogenetic analysis is that the pentaganglionate condition
414
B. DAYRAT AND S. TILLIER
is a synapomorphy of the Euthyneura, secondarily reverted in the Amphibolidae
into triganglionate. Actually, two parietal ganglia occur, as far as known presently,
in only six of the generic taxa mentioned in the present paper; and a right parietal
ganglion alone occurs in three others. This implies that the left and right parietal
ganglia must be treated as two characters, and that the domain of definition must
be defined consequently to test the supposed plesiomorphy of the pentaganglionate
condition within the supposedly monophyletic Euthyneura.
CONCLUSION
The pentaganglionate condition, considered as a general character of the
Euthyneura, is in fact exceptional in statistical terms. Therefore, it cannot be used
as a synapomorphy of the Euthyneura until the history of this character can
be traced through a more comprehensive phylogenetic analysis. By itself, the
triganglionate/pentaganglionate condition does not support monophyly of the Euthyneura, and brings no information on the relationships of their subtaxa with
streptoneuran taxa. The interpretation of so many euthyneuran triganglionate
visceral loops as pentaganglionate probably results from a p i o i acceptance of
evolutionary trends, which have guided interpretations, and sometimes observations.
According to this practice, a triganglionate loop of an euthyneuran gastropod is
essentially pentaganglionate because the pentaganglionate condition is primitive in
Euthyneura; and it is primitive in Euthyneura because the ‘ancestral primitive’
euthyneuran gastropod is Acteon (Fretter, 1939), of which the visceral loop is
pentaganglionate. In this view all the other Euthyneura are derived from an ancestor
having had such a visceral loop and are concealed pentaganglionate.
Our view is that the anatomical observations allow phylogenetic analysis, which
in turn allows firstly constitution of taxa which are evolutionary units, and then
evolutionary interpretation in terms of plesio/apomorphies, history of characters,
history of taxa and scenarios. Evolutionary interpretation follows rather than precedes
observation and constitution of taxa. In taxonomic sampling, the uncritical use of
previous classifications, which in the case of gastropods corresponds to a strong
evolutionary interpretation from ‘primitive’ streptoneuran taxa to ‘advanced’
euthyneuran pulmonates, obliges a pr;oi acceptance, through abusive generalization,
of underlying synapomorphies for which there is no observed justification. This
abuse of generality unavoidably results in a phylogenetic classification which confirms
the previous evolutionary hypotheses. Implementing the domain of definition by (1)
breaking taxa into subtaxa until all groups explicitly used in the data matrix are
monomorphic for all characters, and (2) enlarging the set of taxa of the data matrix
to all the taxa in which the characters are present, as far as necessary, seems to us
the most appropriate way to avoid this circular evolutionary reasoning. Construction
of a data matrix should not be reduced to two steps, i.e. taxonomic sampling
followed by choice and coding of characters. The observation of the variability of
the characters in the initial sample should imply revision of the taxonomic sampling,
independently of the rank of the taxa taken into account, because this rank is a
result rather than a premise of the phylogenetic analysis. The final data matrix
should result from this reciprocal approach.
SAMPLING IN SYSTEMATICS
415
ACKNOWLEDGEMENTS
We are very grateful to Claude Dupuis, Serge Gofas, Guillaume Lecointre, Peter
Mordan, Armelle Sai’hi, and three anonymous referees for help and for critical
comments on the manuscript.
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