Putative speciation events in Lamellodiscus
(Monogenea: Diplectanidae) assessed by a
morphometric approach
TIMOTHÉE POISOT1,2* and YVES DESDEVISES1,2
1UPMC Univ Paris 06, UMR 7628, Modèles en biologie cellulaire et évolutive, Observatoire
Océanologique, 6665, Banyuls/Mer, France
2CNRS, UMR 7628, Modèles en biologie cellulaire et évolutive, Observatoire Océanologique, 6665,
Banyuls/Mer, France
Received 21 July 2009; accepted for publication 18 September 2009 bij_1381 559..569
In the present study, we used morphometry as a proxy to study the microevolution of generalist Lamellodiscus
(Monogenea, Diplectanidae) species, comprising gill parasites of sparid fish. We investigated 147 individuals,
belonging to nine described species, regrouped in four morphotypes. Morphometric measurements were taken on
sclerotized parts of the attachment organ. The formation of groups on the basis of the global morphometry within
a host species, or between several host species, was assessed using both exploratory analyses (principal component
analysis and clustering analysis) and statistical tests. We showed that: (1) for three out of four morphotypes, the
global morphometry was significantly different according to host species used, and (2) the coexistence of two
populations of Lamellodiscus elegans on Diplodus sargus could reflect an ongoing intra-host speciation event. We
suggest that generalist Lamellodiscus are undergoing specialization on their different hosts, which may lead to
speciation. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 559–569.
ADDITIONAL KEYWORDS: generalist – intra-host – monogeneans – morphometry – sparids.
INTRODUCTION
Monogeneans are gill parasites of aquatic organisms,
known to be highly host specific in the wild
(Bychowsky, 1961; Rohde, 1979; Bakke et al., 2007).
However, some genera include generalist species,
parasitizing several hosts species. One example is the
genus Lamellodiscus Johnston & Tiegs (1922), in
which some species can infect up to six hosts from the
fish family Sparidae (Euzet et al., 1993). Desdevises
et al. (2002a) proposed that apparent generalist
Lamellodiscus species could be the result of frequent
host switches, followed by fast speciation events that
are required to maintain a high level of specificity.
This pattern of evolutionary radiation, previously
observed and well documented in Gyrodactylus spp.
(Zietara & Lumme, 2002; Boeger et al., 2003; Meinila
et al., 2004; Huyse & Volckaert, 2005), was suggested
to account for the lack of cospeciation pattern in the
Lamellodiscus–sparid association (Desdevises et al.,
2002a). It was observed that Lamellodiscus are able
to switch hosts in nature (Mladineo & Marsic-Lucic,
2007).
Šimková et al. (2004) suggested that intra-host spe-
ciation is an important mechanism of evolutionary
radiation in Dactylogyrus spp. In this mode of specia-
tion, conspecific populations tend to exploit different
parts of host gills, establishing reproductive isolation
that leads to intra-host speciation (Šimková et al.,
2002, 2006). These events have not received much
consideration in monogeneans because only a few
cases have been investigated to date (Euzet &
Combes, 1980). However, monogenean life-traits (i.e.
*Corresponding author. Current address: Université
Montpellier II, Institut des Sciences de l’Evolution, UMR
5554, Place Eugène Bataillon, 34095 Montpellier CEDEX
05, France. E-mail: tpoisot@um2.fr
Biological Journal of the Linnean Society, 2010, 99, 559–569. With 4 figures
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 559–569 559

direct life cycle, short generation time, high fecundity)
make them prone to intra-host speciation (McCoy,
2003). One method of indicating that such events are
ongoing in a population is to show that infra-
populations (sensu Margolis et al., 1982; Bush et al.,
1997) of a generalist species are different between
host species (if such species are generalist, morpho-
logical difference between groups is expected to be
weak), or that several different populations (e.g. with
different morphometric features) of the same parasite
species coexist in a single host species (intra-host
speciation).
The identification of monogeneans is generally based
on morphological criteria (i.e. qualitative and discrete
characters). Morphometric analysis allows a quantita-
tive approach in the analysis of several body parts of
monogeneans. The hypothesis in the present study is
that a morphometric analysis of several Lamellodiscus
species could help to assess the existence of distinct
populations of generalist species on their different
hosts, as well as the coexistence of several conspecific
populations in the same host species, corresponding to
intra-host speciation. We focused on the opistohaptor
(an organ composed of several sclerotized parts, situ-
ated at the posterior end of the monogenean body) of
Lamellodiscus, which is used by parasites to attach to
host gills. Variations in the length of the different parts
of this organ could be considered as a by-product of
adaptation to the host (Rohde & Hobbs, 1986; Rohde,
1994; Kaci-Chaouch et al., 2008). We did not a priori
assume that differences between groups would be
reflected in a difference in the length of given haptoral
parts (comprising criteria that should be used for
identification), but rather would be reflected by the
existence of distinct morphometric groups, stressing
the need for a multivariate approach.
Lamellodiscus is a convenient model for this type of
study. Recent studies, including one by Amine et al.
(2007b), focused on the description of new species
as morphological variants of previously described
species, thus providing an accurate description of
many morphotypes in the North-Western Mediterra-
nean Sea. However, because these descriptions were
based on the observation of very small changes in the
morphology, the species status of most of these new
Lamellodiscus is questionable. Moreover, these differ-
ences are not consistent, nor discrete, and it is possible
to find individuals forming a continuum of shapes
between two alleged species. Because of the existence
of such a continuum, it is sometimes difficult to deter-
mine to which species a given individual belongs, and
we considered it more correct and more conservative
to group all species sharing a high level of
morphological similarity into a reduced number of
morphotypes. Moreover, as previously noted, some
Lamellodiscus species have substantially larger host
ranges compared to other monogeneans, thus allowing
the investigation of putative morphometrical differ-
ences between populations on different hosts species.
The analysis of 147 Lamellodiscus individuals from
nine described species allowed us to demonstrate sig-
nificant morphometric differences within generalist
parasites between their different hosts for three mor-
photypes (named with respect to the group’s most
characteristic species): Lamellodiscus elegans, Lamel-
lodiscus kechemirae, and Lamellodiscus ergensi. We
propose that these morphometric differences indicate
radiation via a host switch followed by speciation. In
addition, we show the existence of sub-populations on
some hosts within a parasite species, potentially sup-
porting a sympatric speciation event.
MATERIAL AND METHODS
FISH AND PARASITE SAMPLING
Fish were captured in the Golfe du Lion, near
Banyuls-sur-Mer (42°28′47″N, 3°08′10′E), by free-
diving. To ensure that hosts were sampled in the
same community, the sampling area was kept inferior
to 1 km2, at a depth less than 15 m. Sampling was
conducted under constant environmental conditions
(q ª 20 °C, salinity ª 37.5 PSU) because the environ-
ment has been suggested to affect the development of
monogeneans (Mo, 1991, 1993; Dmitrieva & Dimitrov,
2002). Immediately after capture, each fish was killed
by a sharp shock on the top of the head. Gills were
removed and kept in cooled sea water until parasite
sampling (maximum of 30 min after capture). Twenty
fish, belonging to seven species (Diplodus sargus,
Diplodus vulgaris, Diplodus annularis, Diplodus
puntazzo, Oblada melanura, Salpa salpa, and
Lithognathus mormyrus) were examined (Table 1).
Gills were screened under an Olympus SZ61 stere-
omicroscope, and Lamellodiscus individuals were col-
lected alive. Identification was carried out with an
Olympus CX41 light microscope. Gill screening
occured no more than 2 h after fishing.
MORPHOMETRIC ANALYSIS
Lamellodiscus individuals were mounted on a slide
with 2.5% sodium dodecyl sulphate, after a modifica-
tion of the protocol described by Wong et al. (2007), to
enable a clear visualization of the sclerotized parts,
thus allowing greater precision during measurements.
A picture of the haptor of each parasite was taken
using a Sony Exwave HAD digital camera mounted
on an Olympus CX41 light microscope, at ¥400
magnification. Images were loaded into IMAGEJ
(Abramoff et al., 2004) to perform measurements.
Measurements were taken using the landmarks
method by taking distances between two points
560 T. POISOT and Y. DESDEVISES
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 559–569

(Fig. 1). The mean ± SD for each measurement (for
each morphotype, on each host) are provided in the
Supporting Information (Table S1).
Species were grouped into four morphotypes on the
basis of a high level of morphological similarity. Simi-
larity was defined by reviewing the shapes of the
haptoral parts (mostly median ventral and lateral
dorsal bars) and male copulatory organs, and species
differing only in minor details were grouped. The
composition of the morphotypes was (1) Lamellodiscus
ignoratus s.l. L. ignoratus s.s., L. confusus, L. neifari,
L. falcus; (2) L. ergensi: L. ergensi, L. tomentosus. Two
other morphotypes are formed by a single species; (3)
L. kechemirae and (4) L. elegans, whose morphology is
clearly differentiated from the others Lamellodiscus
species.
Table 1. Host–parasite associations investigated
Diplodus
sargus
(7)
Diplodus
vulgaris
(6)
Diplodus
puntazzo
(1)
Diplodus
annularis
(3)
Oblada
melanura
(1)
Lithognathus
mormyrus
(1)
Salpa
salpa
(1)
Lamellodiscus
ignoratus s.l.
23 11 2 1 10 4
Lamellodiscus elegans 33 10 2 5
Lamellodiscus ergensi 12 5 6 *
Lamellodiscus
kechemirae
6 16
*Association reported in the literature (Desdevises et al., 2002a; Amine et al., 2007b), but not found in our sample.
Composition of the morphotypes: L. ignoratus s.l. L. ignoratus s.s., L. confusus, L. neifari, L. falcus; L. ergensi: L. ergensi,
L. tomentosus; L. kechemirae and L. elegans are individual species. The number of sampled host individuals is reported
in the first line. Numbers in the body of the table indicate the occurrence of each association (number of parasites in a
given host species) in our sample.
a
b
c g
f
d
mvb
ldb
c’
b’a’
Figure 1. Overview (upper part) and measurements (lower part) of the haptor of Lamellodiscus (ignoratus type,
lamellodiscs and marginal hooks are not shown). mvb, median ventral bar; ldb, lateral dorsal bar; a, a′, length of hamuli;
b, b′, point length; c, c′, hook opening; d, guard opening; f, root length; g, guard length.
PUTATIVE SPECIATION EVENTS IN LAMELLODISCUS 561
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 559–569

STATISTICAL ANALYSIS
P < 0.05 was considered statistically significant.
Analyses were performed using the R 2.9.1 (R Devel-
opment Core Team, 2008). Homogeneity of variances
was first tested using Bartlett’s test by permutation
(999 permutations) to determine which test was to be
subsequently used. Permutational tests were used
when variances were homogeneous, and nonpara-
metric tests were used otherwise (Sheskin, 2004).
Preliminary investigation
Preliminary studies using a subset of our data, via
measurements on nonfixed and unflatenned para-
sites, allowed us to rule out the hypothesis that
variability in haptoral part lengths is driven by para-
site size because there is little correlation between
body size and most of the other measurements (see
Supporting Information, Table S2). Moreover, prepa-
ration for observation under a light microscope tends
to flatten the parasite’s body, making measurements
of total body length potentially unreliable. We there-
fore chose not to include this variable in our analyses.
Exploratory analysis
Two exploratory methods were used to assess mor-
phometrical differences between or within host
species. First, a principal component analysis (PCA;
Legendre & Legendre, 1998) was conducted using all
variables measured on the haptor. Second, the Euclid-
ian standardized morphometric distance between
individuals of L. elegans found on D. sargus was
computed using all measurements made on the
haptor, and a clustering analysis was carried out,
using the unweighted pair group method with arith-
metic mean, implemented in APE (Paradis et al.
2004) on all morphometric distances after standard-
ization. The reliability of each node of the dendro-
gram, which is assumed to be an indication of the
difference between the groups, was estimated using a
nonparametric bootstrap analysis (1000 replicates).
Quantification of differences between groups
To test whether or not the global morphometry of
parasite individuals from the same species were sig-
nificantly different between hosts, we extracted the
first component of the PCA, which was considered as
an integrative variable, summing up the morpho-
metry of each individual (hereafter refered to as the
‘morphometric value’). A comparison was made
between hosts using the Kruskal–Wallis test (a
Mann-Whitney test was used when there were only
two groups to compare; Sokal & Rohlf, 1995).
When exploratory analyses revealed the existence
of two populations of a parasite species within a
single host species, their morphometric values were
compared using a Student’s t-test, with 999 permu-
tations. The Hartigan–Hartigan dip test of unimodal-
ity (Hartigan & Hartigan, 1985) was applied to
ensure that the distribution of morphometric values
was truly bimodal.
Variance comparison
To assess whether the variability of populations of L.
elegans on D. sargus was comparable with the values
found for specialist Lamellodiscus species, variances
for each morphometric character were computed for
each sub-population of L. elegans on D. sargus, and
compared with the variance of the whole population
of L. elegans on D. sargus. Values were also compared
with weighted average variances found by Kaci-
Chaouch et al. (2008). Variances were compared with
F-tests, and the F-statistic was doubled to control for
a type 1 error (Bruning & Kintz, 1987).
RESULTS
One hundred and forty-seven Lamellodiscus parasites
belonging to nine putative Lamellodiscus species
were regrouped into four morphotypes based on high
morphological similarity (for distribution of morpho-
types on host species, see Table 1).
We consider that the value for the first component
is summing up the morphometry of each individual
because of the high percentage of variance explained
[eigenvalue of the first axis for each morphotype (%):
L. elegans = 74.5; L. kechemirae = 54.5; L. ignoratus
s.l. = 71.1; L. ergensi = 66.7]. No correlation was found
between host size and morphometric value (for all
parasites together as well as for each morphotype).
Out of the four morphotypes, only three presented a
significant difference in morphometry between the
different hosts (Fig. 2): L. ergensi (P = 0.003), L.
elegans (P = 0.007), and L. kechemirae (P = 0.02). No
significant difference was found for L. ignoratus
(P = 0.19). However, the comparison of morphometry
of L. ignoratus from D. puntazzo and L. mormyrus
showed a significant difference (P = 0.03).
Two populations of L. elegans on D. sargus were
observed (Fig. 3). However, these two L. elegans popu-
lations were not found on the same D. sargus host
individual. The difference between means in morpho-
metric value was tested using a Student’s t-test with
999 permutations, and was found to be significant
(P = 0.0001). This fragmentation in two groups is
visible on the dendrogram built using morphometric
distances (Fig. 4). Bootstrap values delineate two
groups of L. elegans individuals within the same host
species (with an internal branch with 100% bootstrap
support). Within each group, the branches are poorly
supported, which indicates that the global population
of L. elegans on D. sargus is formed by two morpho-
562 T. POISOT and Y. DESDEVISES
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metricaly distinct sub-populations, each one being
homogeneous. Variances for L. elegans on D. sargus
(Table 2) are similar to those found for specialist
species [L. virgula, L. baeri, L. drummondi, L. eryth-
rini, except for the root length (f) and the dorsal
hamuli length (a′) in sub-population 1, and root (f)
and guard (g) length for sub-population 2; Fig. 1],
whereas the variance of the whole population was
similar to the one found for generalist species (except
for the length of the median ventral bar). Moreover,
the distribution of morphometric values of L. elegans
on D. sargus is significantly different from unimodal-
ity (Dip > 0.1).
DISCUSSION
Morphometric analysis has already been used in
several monogenean genera. Shinn et al. (2001) used
morphometric tools to discriminate between the
pathogenic Gyrodactylus salaris and other congeneric
species on salmonids. Similarly, Mariniello et al.
(2004) differentiated several species of Ligophorus,
and demonstrated considerable morphological varia-
tion between allopatric populations of Ligophorus
angustus. Huyse & Volckaert (2002) used morphom-
etry to reveal the existence of a species complex
within Gyrodactylus spp. However, these studies were
mostly descriptive, and did not use morphometric
analysis to assess diversification below the species
level.
Kaci-Chaouch et al. (2008) showed that, within
Lamellodiscus, morphometric variability was higher
in generalist than in specialist species. Beyond this
result, the present study emphasizes that, except for
L. ignoratus, generalist Lamellodiscus species are not
similar (in their morphometry) on their different
hosts, but tend to form clusters (Fig. 1). The observa-
tion that L. ignoratus is the morphotype with the
greatest host range (Euzet et al. 1993) could account
for the lack of group formation if the rate of special-
ization is not equal in all host species, or if special-
ization is not occurring in all host species. This
D. puntazzo
(C) (D)
(B)(A)
D. sargus D. vulgaris
−
8
−
6
−
4
−
2
0
2
D. sargus D. vulgaris O. melanura−
6
−
4
−
2
0
2
4
D. sargus D. vulgaris
−
4
−
2
D. puntazzo D. sargus D. vulgaris L. mormyrus S. salpa
−
6
−
4
−
2
0
2
4
4
2
0
Figure 2. Differences in morphometrics in the four Lamellodiscus morphotypes on different hosts (Diplodus putazzo, D.
sargus, D. vulgaris, Oblada melanura, Lithognathus mormyrus, and Sarpa salpa). After Kruskal-Wallis test, morpho-
metrics are different between hosts for Lamellodiscus ergensi (A), L. elegans (B) and L. kechemirae (C), but not for L.
ignoratus (D).
PUTATIVE SPECIATION EVENTS IN LAMELLODISCUS 563
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statement is confirmed by the fact that L. ignoratus
on Diplodus puntazzo and Lithognathus mormyrus
are morphometrically different. Desdevises et al.
(2002a) suggested a host switch followed by speciation
as the main mechanism of evolutionary radiation in
Lamellodiscus. Therefore, depending on the age of the
association (time at which the host was acquired),
specialization may not have started yet. This result
also indicates that inter-host speciation, although
readily found in our association, is in no way a
general trend, and that specialization is not the
unavoidable result of the exploitation of several hosts.
The morphometric analysis revealed the existence
of distinct groups of a parasite species within a host
species: L. elegans on D. sargus. This result can be
interpreted in several ways (Brooks & McLennan,
1993; Poulin, 1999; McCoy, 2003). It could be an
indication that two populations of hosts are coexisting
in the study area, each harbouring a distinct parasite
population, stressing the need to consider hosts when
studying parasite populations (i.e. the host population
might not be homogeneous; Secord & Kareiva, 1996).
This claim is supported by the fact that none of
the hosts investigated during the present study
carried parasites from both sub-populations (Fig. 4).
However, without more work on the host population,
trying to determine which host features account for
this heterogeneity would remain speculative. Intra-
host speciation has been studied in Dactylogyrus spp.,
and it was suggested that specialization to exploit
different parts of host gills (reflected by the modifica-
tion of morphometric characters in the parasites) was
a factor initiating speciation (Šimková et al., 2002,
2006). In the case of L. elegans on D. sargus, the
observed separation in two populations could be
linked to an adaptation to different parts of the gills
(Šimková et al., 2004).
An alternative hypothesis is that host populations
might have been geographically isolated at some
time, and then undergone a secondary contact, trig-
gering resource partioning among the parasites. In
this situation, we expect to observe the same pattern
D. sargus 1
D. sargus 1
D. sargus 2
D. sargus 2
D. sargus 2
D. sargus 3
D. sargus 3
D. sargus 3
D. sargus 6
D. sargus 6
D. sargus 7
D. sargus 7
D. sargus 7
D. sargus 7
D. sargus 7
D. sargus 8
D. sargus 8
D. sargus 8
D. sargus 8
D. sargus 9
D. sargus 9
D. sargus 9
D. sargus 9
100
90
37
62
63
53
57
43
39
8
99
44
14
85
12
7
38
31
68
11
H
osts 1, 8 and 9
H
osts 2, 3, 6 and 7
Figure 4. Dendrogram reconstructed using the unweighted pair group method with arithmetic mean on the standardized
Euclidian distances based on morphometric variables between individuals of the morphotype Lamellodiscus elegans on
Diplodus sargus. Each host is identified by a number. The two sub-populations are formed by parasites from different
hosts. Node labels indicate bootstrap values (1000 replicates, expressed in %). Hosts identification numbers are given for
information purposes.
PUTATIVE SPECIATION EVENTS IN LAMELLODISCUS 565
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as in true sympatric speciation. A more thorough
study of this association is required to investigate this
idea. The fact that the two populations of L. elegans
on D. sargus are not evenly distributed on all hosts
but, instead, correspond to two groups of hosts, sug-
gests that this speciation is not ongoing at the intra-
host level: if the factor initiating speciation is
specialization in the exploitation of different parts of
the gills, one would expect to find individuals from
each population within the same hosts. The finding in
the present study could also be explained by the fact
that L. elegans parasites from D. sargus are under-
going an intra-host speciation event, resulting in the
emergence of two groups that are distinguishable by
their morphometry. The low bootstrap values within
sub-groups suggest that the individuals within each
group are homogeneous on the basis of their global
morphometry.
As previously noted, recent descriptions of Lamel-
lodiscus species have been based on very small and
sometimes inconsistent morphological differences
(Amine et al., 2007a, b). The results obtained in the
present study did not reveal morphometric groups to
support these species distinctions, raising doubt as to
their validity. However, we did not use the samples of
Amine et al. (2007a, b), nor did we sample in the same
geographic area. Because it has been suggested that
monogeneans are good models to study speciation and
adaptation to the host (McCoy, 2003), the results
obtained in the present study emphasize that it is
important to be especially careful when describing
new monogenean species. This issue needs to be more
thoroughly investigated using molecular data.
Morphometric variability was shown to be a good
correlate of host-specificity in Lamellodiscus (Kaci-
Chaouch et al., 2008). We found that L. elegans on D.
sargus (1) forms two sub-populations and that (2)
within each sub-population, the morphometric vari-
ance is similar to the weighted average variance
found for specialist Lamellodiscus species. This
finding supports an ongoing intra-host speciation
event, reflected by an adaptation, either to different
parts of the gills or to different host populations.
However, an exhaustive analysis of how Lamellodis-
cus individuals distributes on the gills of their hosts,
which would allow one of these hypotheses to be ruled
out, remains to be conducted. We found that variance
within each sub-population of L. elegans on D. sargus
was similar to the weighted average variance of spe-
cialist Lamellodiscus species, whereas the variance
for the whole population was similar to the variance
observed for generalist Lamellodiscus species. Kaci-
Chaouch et al. (2008) suggested that morphometric
variability within generalist species was higher than
within specialist species. The results obtained in the
present study suggest that the greater variance
observed in generalist species is a result of their trend
to form groups, even within a host species. The dif-
ference of variance between generalist and specialist
species could be at least partially a result of this
group formation in generalists, which is not observed
in specialists (Kaci-Chaouch et al., 2008), thus sug-
gesting that different factors act in phenotypic evolu-
tion in generalist and specialist species. Moreover,
whether the host–parasite assemby is formed by colo-
nization or descent might impact group formation,
and remains to be investigated.
A similar phenomenon could act for generalist
species between their different hosts. The formation
of groups, according to morphometry, could indicate
an adaptation to each host species, leading to special-
ization. This result is consistent with the study by
Desdevises et al. (2002a) claiming that evolutionary
radiation in Lamellodiscus is the result of a host
switch followed by speciation. Desdevises et al.
(2002b) suggested that specialization in Lamellodis-
cus is not an evolutionary ‘dead-end’, but rather an
ancestral state, and that Lamellodiscus species tend
to acquire new hosts. The observation that individu-
als belonging to generalist species are forming groups
on at least some of their different hosts may reflect
ongoing specialization events, along with adaptation
to the new hosts.
The clustering of individuals according to different
hosts may be seen as phenotypic plasticity. Current
knowledge, however, does not support this hypothesis.
Previous studies focusing on phenotypic plasticity of
haptoral parts (Mo, 1991, 1993; Matejusová et al.,
2002) indicate that this phenomenon, when detected,
does not induce variations of the same amplitude to
that observed in the present study (i.e. several factors
are also known to modify the size of haptoral parts;
Ergens & Gelnar, 1985, Dmitrieva & Dimitrov, 2002),
although additional work is needed to investigate the
role of phenotypic plasticity in morphometric varia-
tion because this phenomena alone could explain the
pattern observed in the present study. In the case
of phenotypic plasticity, no genetic differentiation
between parasite populations would be seen, as would
exist in the case of true differentation following assor-
tative mating. Because we ensured that environ-
mental conditions known to potentially impact the
development of sclerotized parts of monogeneans
were constant during sampling, the results obtained
support the hypothesis that the observed differences
are a result of the host. However, the possibility
remains that the hosts studied belong to populations
that have experienced different environmental condi-
tions in the past. Even in morphotypes in which
morphometry suggested the existence of different
groups, no single discriminant morphological feature
could be used to identify these groups. However, the
566 T. POISOT and Y. DESDEVISES
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objective of the present study was to assess the exist-
ence of groups within, and not between, species.
Moreover, even in studies indicating that pheno-
typic plasticity might be acting in some monogenean
genera, parasite populations were not different
(according to morphometry) between their hosts (e.g.
Paradiplozoon homoion; Matejusová et al., 2002). The
fact that speciation would be reflected in modification
of the size of haptoral parts can be seen as a conse-
quence of a strong evolutionary pressure acting on the
shape of the haptor, resulting in a better adaptation
to host. One might also expect that competition
between different Lamellodiscus populations within a
single host would affect their development, and could
introduce nonhost-induced variation in the length
of haptoral parts. However, many studies (Euzet &
Combes, 1998; Morand et al., 1999; Šimková et al.,
2000, 2001b; Lo & Morand, 2001; Rohde, 2002) have
suggested that monogenean niches are not saturated,
indicating that competition is low or absent amongst
monogeneans. However, these studies mostly relate to
interspecific competition, and intraspecific competi-
tion is far less known in monogeneans. We cannot
rule out its possible effects on parasite development.
Futuyma & Moreno (1988) stressed that causes and
consequences of specialization should be considered
distinctly. However, this distinction is not always
straightforward (especially in the case of morphom-
etry): adaptation to a host may be the result of
specialization driven by other factors (thus being a
consequence) but could also be a constraint for further
specialization (thus acting as a cause). It is known
that specialist monogeneans are found on larger hosts
compared to generalists (Sasal et al., 1999; Šimková
et al., 2001a; Morand et al., 2002; Desdevises et al.,
2002b). Because size is a life-trait correlated with
longevity and proximity to the top of the food web
in fish (Winfield & Nelson, 1991; Winemiller &
Rose, 1992), this finding supports the hypothesis of
specialization on predictable resources (Ward, 1992).
However, the fact that generalist species tend to form
clusters on their different hosts was not taken into
account in these studies and should receive proper
attention in any future investigations.
Finally, morphometrics alone cannot fully answer
the question of the occurrence of speciation events,
and some other factors may play an important role.
Chemical stimuli from the host are responsible for
recognition by oncomiracidium (Buchmann & Linden-
strøm, 2002), and the host triggers an immune
response against the parasite (Jones, 2001), especially
during parasite growth (Faliex et al., 2008). Before
morphometry could act in host–parasite compatibility,
these factors may modify the encouter or compatibil-
ity filters defined by Combes (2001), thus regulating
specificity, the potential for the the acquisition of new
hosts, and the chances for the parasite to properly
develop on its host. Moreover, anterior adhesive areas
play a role during infection (Whittington et al., 2000).
Changes in factors regulating the infection of host by
infective stages are certainly important in the deter-
minism of specificity, whereas morphometry could at
least in part be a consequence of such changes. In
addition, it is possible that parasite morphometry is
influenced by the biology of the host (e.g. via host
populations fragmentation leading to parasites’ mor-
phometric divergence, followed by a mixing of these
host populations in a sympatric distribution).
However, investigating this point requires an exten-
sive amount of data on host populations.
In summary, a morphometric analysis of 147 gener-
alists Lamellodiscus individuals on seven sparid host
species revealed the existence of four morphometric
sub-groups. Most of these groups were associated with
the host species from which the parasites were recov-
ered, suggesting that some generalist parasites could
be undergoing an allopatric (inter-host) speciation
event. Interestingly, we identified the existence of two
subgroups of L. elegans on the same host species (D.
sargus), which may represent a sympatric speciation
event. By contrast, some generalist parasites (e.g. L.
ignoratus) did not show morphometric group–host
associations, suggesting that some generalist para-
sites do not represent intermediate forms at present.
ACKNOWLEDGEMENTS
We are grateful to Pascal Romans for invaluable help
in fish sampling. We thank Louis Euzet for a discus-
sion on the different morphotypes that we encountered
during this work; Pierre Legendre and Daniel Borcard
for their help with implementation of permutation
tests; and Emmanuel Paradis for his assistance during
application of nonparametric bootstrap to our data. We
thank Jean-Lou Justine and two anonymous referees
for their insightful comments on the manuscript.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article:
Table S1. Mean and variance of morphometric values for all parasite morphotypes.
Table S2. Correlations between length of haptoral parts.
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