Morphological and genetic differences in ecologically distinct

Biological 30uml .f the Linnean Society (1992),47: 49-60. With 6 figures
Morphological and genetic differences in
ecologically distinct populations of Petrosia
(Porifera, Demospongiae)
GIORGIO BAVESTRELLO AND MICHELE SARA
Istituto di <oologia dell'llniversitci, Via Balbi, 5-I 16126 Genova
Received 7 August 1990, accepted for publication 8 3anuory 1991
The taxonomic status of two sponge morphotypes living sympatrically in Mediterranean caves and
usually ascribed to PctroszaJiciformis was elucidated on the basis of morphological, morphometric and
genetic features. The two morphotypes, spherical and cylindrical, showed differences in the shape
and size of spicules and in the morphology of the aquiferous system. Electrophoretic analyses
demonstrated that the two morphotypes are reproductively independent and so they should be
considered as distinct biological species. The spicular features allow attribution of the cylindrical
morphotype to P.&iformLr and the spherical one to P. clauata. For these two species parasympatric
speciation is proposed.
KEY WORDS:-Polymorphism - morphometry
marine sponges - Mediterranean Sea.
-
electrophoresis
-
parasympatric speciation -
CONTENTS
Introduction . . .
Materials and methods
Results
. . . .
External morphology
Aquiferous system.
Spiculation . .
Electrophoresis .
Discussion.
. . .
References. . . .
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INTRODUCTION
The traditional taxonomy of sponges, based on spicule morphology, often
seems inadequate. Anatomical, histological, cellular, reproductive and chemical
characteristics are utilized additionally to delimit super-specific taxa (Bergquist
& Wells, 1983; Bergquist, 1980; Simpson, 1969; Levi, 1956, 1973).
The inadequacy of traditional taxonomic criteria is particularly evident for
some groups, such as the Haplosclerida and allied orders, because of the paucity
and variability of the available characters (De Weerdt, 1985). Therefore, a more
comprehensive approach may be used utilizing traditional spicular features and
also such features as the architecturae of aquiferous system (Sara & Manara, 1991;
0024-4066/92/090049
+ 12 SOS.OO/O
49
0 1992 The Linnean Society of London
50
G. BAVESTRELLO AND M. SARA
Bavestrello, Burlando & Sara, 1988) and the electrophoretic analyses of genetic
markers (Sol&-Cava & Thorpe, 1986, 1987; Soli-Cava & Thorpe, 1991;
Soli-Cava, Thorpe & Manconi, 1991; Sara etal., 1989; Stoddart, 1989). A
similar approach has been utilized successfully in different groups of marine
invertebrates (for example, see Shaw, Beardmore & Ryland, 1987; Carter &
Thorpe, 1981; Manwell & Baker, 1963; Grassle & Grassle, 1976).
I n this work morphological and electrophoretic analyses were carried out to
elucidate the taxonomic status of the morphotypes usually ascribed to Petrosia
j c i f r m i s (Poiret) living in Ligurian marine caves.
Sara & Vacelet ( 1973) described two different morphotypes of Petrosia living
in sheltered habitats: cylindrical, creeping specimens living under overhanging
rocks and spherical, small specimens living in dark caves. A third morphotype
comprising mushroom-like specimens lives on rocky cliffs exposed to high levels
of water movement and solar radiation.
Usually, all the Mediterranean Petrosia as ascribed to P.Jiciformis but in a
recent work on Mediterranean demospongiae, Pulitzer-Finali ( 1983) identified
three samples recorded from the Bay of Naples and from Portofino as P. clauata, a
species synonymous with P.Jici$ormis according to Topsent (1934).This species is
distinguished from P.jciformis by the smaller spicule size and by the lack of short
reniform oxeas and strongyles. The present study aims to clarify the biological
status of these species on the basis of morphological and genetic characteristics.
MATERIALS AND METHODS
Samples of ten specimens of both cylindrical and spherical morphotypes of
Petrosia were collected by SCUBA diving in August 1988 at Paraggi, Zoagli and
Bergeggi (Ligurian Sea) (Fig. 1 ) . All the specimens were taken in the same
period in order to reduce the spicular variability caused by seasonal growth
patterns (Jones, 1987; Fry, 1968). Cylindrical specimens were collected from the
lighter parts of caves whereas spherical ones came from the dark parts. In the
intermediate areas of the caves exist overlapping zones where both morphotypes
are present. The studied populations are represented by a low number of
randomly distributed specimens without evident formation of groups of
clonema tes.
For the morphometric analyses of the spicules two slides were prepared from
each specimen. Spicules were measured by light microscope using a camera
lucida and ‘Graphtec’ digitizer (Jones, 1987). The average spicule size in the
populations was calculated and the differences tested by t-test. For oxeas, the
most abundant category of spicules, the width/length ratio was calculated.
Some specimens of each morphotype were used for production of corrosion
casts (similar to those commonly used in anatomical studies of vertebrate
vascular organs) of the aquiferous system. This technique provides for the
injection of a plastic resin through the oscules (Bavestrello, Burlando & Sara,
1988). T h e casts were analysed by stereo microscopy and scanning electron
microscopy in order to obtain a detailed reconstruction of the canal system.
The specimens utilized for spicular studies (from Paraggi and Zoagli) were
also analysed by Cellogel electrophoresis for 15 enzyme systems. This last
analysis was not carried out on the Bergeggi samples because we obtained only
fixed material, unsuitable for electrophoretic analysis, from this population.
DIFFERENCES IN POPULATIONS OF PETROSZA
PBergeggi
. _.
P
51
--
. ...--a.
LIGURIAN SEA
Figure 1. Localities sampled.
Only nine loci could be recorded consistently for all populations. This is
probably due to the low concentration of enzymes in sponge tissue (Sol&Cava &
Thorpe, 1987; Solt-Cava, Thorpe & Manconi, in press). The methods
employed are similar to those described by Richardson, Baverstok & Adams
(1986) and used for sponges by Sara et al. (1989). The loci scored were GPgd,
Mpi, Hk, Mdh, Pgi, Es, Ak, Got and Tr. Allelic frequencies and Nei's (1972) I and
D indices were calculated.
RESULTS
External morphology
T h e main morphological features of the collected specimens are summarized
in Table 1.
T h e volume of spherical specimens is quite constant while cylindrical
specimens show wider dimensional variation. This may be due to the tendency of
these specimens to form an anastomosing network in which different individuals
can be fused. T h e volume/oscular area ratio is relatively constant in both
morpho types.
TABLE
I. External morphology. Based on 10 specimens of each morphotype at each locality
Locality
morphotype
Bergeggi
Zoagli
Paraggi
-
Spherical
Cylindrical
Spherical
Spherical
Cylindrical
~
Volume (ml)
Oscular area (mm')
No of oscules
Density (g ml-')
Silica contents (%)
Colour
4.552.5
7.27i5.04
1-2
0.066
45.2k8.7
White
21.45+ 14.01
21 k12.34
3-5
0.063
52.3k9.1
Whi te-viole t
10.9f9.57
9.86k8.39
1-2
0.06
50.4f 16
White
13.07k4.9
1 1.35 f4.25
3-6
0.082
47+ 16
White-violet
Cylindrical
~~
6.9+ 1.9
7.61k3.15
1-2
0.068
53 k9.8
White
6.75k 1.48
11.97k5.22
4-9
0.072
55+18
White
52
G. BAVESTRELLO AND M. SARA
Figure 2. Diagram showing the architecture of the main inhalant canals in the two morphotypes.
A, Spherical morphotype. B, Cylindrical morphotype. The dashed line indicates the sponge surface.
Arrowheads: incurrent canals. Arrows: subdermal spaces.
Aquiferous system
Bavestrello et al. (1988) described the canal system of mushroom like
morphotypes of Petrosia ficiformis. This morphotype shows an anastomatic,
superficial network of canals in communication with ostia, determining a
subdermal space (Simpson, 1984). A system of canals distributes the water from
the superficial network to the choanosome. The excurrent system is a series of
modules radiating from the atrial cavity and branching in the choanosome.
Large incurrent canals frequently merge with the excurrent ones deep inside the
sponge body and at the superficial level. Spherical specimens, coming from the
dark part of caves (Fig. 2A), show little variation in the structure of the
aquiferous system while greater variability can be detected in the canal system of
the cylindrical morphotype. The latter does not show the incurrent network
surrounding the whole sponge but single tree-like incurrent organs which are
separate structures at the surface of the sponge (Fig. 2B). For this reason the
cylindrical specimens d o not show, in section, the typical subdermal space of the
other morphotypes.
Spiculation
Spicular composition
The spicules found in the genus Petrosia comprise distinct categories of
megasclere with respect to both size and type: oxeas, styles and strongyles
isodiametric large and thick, short and reniform oxeas and strongyles are always
present (Bergquist & Warne, 1980; Pulitzer-Finali, 1983; De Weerdt, 1985;
Desqueiroux-Faundez, 1987).
DIFFERENCES IN POPULATIONS OF PETROSZA
53
50
0
Cyl.
Spher.
Spher.
PARAGGI
Oxeas
0
Figure 3. Spicular composition
Styles
Cyl.
ZOAGLI
Cyl.
BERGEGGI
Spher.
Strongyles
(yo)of the two morphotypes from the sampled localities.
In our study we divided the spicules into three categories: oxeas, styles and
strongyles. In each spicule slide we counted the number of spicules belonging to
each type. Oxeas were always the main category (80-99%) (Table 2), styles and
strongyles were either sparse or well represented. At Paraggi and Bergeggi the
percentage of oxeas is greater in the spherical morphotype (Fig. 3) but this
difference is statistically significant only at Paraggi (t-test, 0.05 > P > 0.01). At
Zoagli the two morphotypes showed the same spicular composition.
Size of spicules
This study, based on about 600 spicule measurements for each population,
shows a complex pattern of differences among localities and morphotypes
(Table 2). The spicules of specimens from Bergeggi were bigger than those from
the other localities (Fig. 4), while the Paraggi and Zoagli specimens showed
similar spicule size. In spite of this interpopulation variability, differences in size
between the two morphotypes were always detected (Fig. 4).The size of spicules
of the cylindrical morphotypes is consistently greater in all the localities studied.
The lack of significance of some differences regarding strongyles is probably due
to the small number of such spicules in our slide.
The average volume of oxeas, calculated according to Jorgensen (1944), is
5004-8746 pm3 for the spherical morphotype and 12 977-23 568 pm3 for the
cylindrical. Since the amount of silica is quite constant in the two morphotypes
(Table 1) the spherical morphotype has, in the same volume, 1.5-4.5 times the
number of spicules found in the cylindrical morphotype.
Widthllength ratio
This ratio is useful in that it gives a comprehensive description of the general
shape of monoaxonic spicules. The average values of the ratio in each length
class, plotted against the length of spicules, allows us to compare the shape
differences at each developmental stage (Fig. 5).
In Bergeggi and Paraggi the values of the ratio are greater in the cylindrical
morphotype than in the spherical one while, in Zoagli, no significant differences
between the two morphotypes were detected (Fig. 5). In Bergeggi and Paraggi
the differences are particularly strong in the small classes of spicules. This is due
Volume
of oxeas (pm3)
(yo)
5339f 1318
12
82
6
6.18k2.51
7.88 f 2.46
7.66f2.57
Width (pm)
Oxeas
Styles
Strogyles
Types of spicules
Oxeas
Styles
Strogyles
177.81 k51.93
178.66k41.42
93.23k 57.55
k n g f h (pm)
Oxeas
Styles
Strogyles
Spherical
Cylindrical
11968f3432
69
11
20
8.66f 5.41
9.14f 2.99
8.54k 2.74
203.53+ 70.88
190.88k55.97
93.18f60.62
Paraggi
9370f2410
86
4
10
8.28+ 2.30
7.97k2.10
8.40f 3.12
174.lOk47.13
118.65f44.73
83.69539.45
Spherical
Cylindrical
13697k3750
86
9
5
8.92 k 3.19
10.39k2.48
9.81 f2.19
219.30k61.56
215.19f64.19
174.78f80.2
Zoagli
TABLE
2. Morphometry of spicules
7638 f2061
1
95
4
6.95 f3.02
8.01 f2.64
8.53f2.17
201 6 2 k 5 1 . 7 0
197.65f45.41
1 15.46k62.2
Spherical
Cylindrical
24877 f5629
91
2
7
11.30 k 3.92
10.63+2.40
10.52f 2.65
248.27 f79.28
150.84k68.80
134.51 f53.43
Bergeggi
3..
P
5
3
rP
t;
Er
2
c
c,
DIFFERENCES IN POPULATIONS OF PETROSIA
Strongyles
Oxeas
40(
Length
T
T
I
I
T
0
Width
15
c
55
I T
PAR
ZOA
Cyl ind r ica I
1I
BER
Width
PAR
ZOA
BER
0
Spherical
Figure 4. Average sizes of oxeas and strongyles in the two rnorphotypes from the sampled Iocalities;
bar represents & standard deviation; (*) L-test, 0.05 > P > 0.01.
to the presence of the short and thick oxeas that Pulitzer-Finali (1983)
considered typical of P.Jic$orrnis: these were lacking in Zoagli specimens.
Electrophoresis
Loci where all the tested specimens gave reliable results are listed in Table 3.
The data show that all populations are monomorphic for the same allele at three
loci (Es, Mpi and Tr) while the other loci show varying amounts of
polymorphism. The 6Pgd and the Ak loci are monomorphic for different alleles in
the two morphotypes for Paraggi and Zoagli.
The genetic identity within the same morphotype is high ( I = 0.903 between
spherical populations of Zoagli and Paraggi and I = 0.956 between cylindrical
populations of Zoagli and Paraggi), while it is low between the two morphotypes
( I = 0.62 between cylindrical and spherical populations) (Fig. 6). These facts
suggest reproductive isolation and a high genetic divergence between the
examined morphotypes.
G. BAVESTRELLO AND M. SARA
56
O’I4r
IA
Bergeggi
-
320
0.2 L
Zoaqli
-
01
40
I
I
I
I
I
I
I
I
I
I
I
I
I
30C
Figure 5. Average values of oxeas width/length ratio in each class of length in the two morphotypes
from the sampled localities; bar represents the standard deviation; ( * ) t-test, 0.05 > P > 0.01.
DISCUSSION
We show that in the Ligurian sheltered habitats two reproductively isolated
forms of Petrosia distinguishable by morphological and spicular features are
present. The genetic distance shown by the electrophoretic analysis suggests that
these two forms may be considered as different biological species.
In Table 4 the specific characteristics of P.jciformis and P . clavata described by
Pulitzer-Finali (1983) are compared with the features of the cylindrical and
spherical morphotypes. Differences in spicule size and composition as well as
DIFFERENCES IN POPULATIONS O F PETROSIA
57
I
I
0.9
0.8
0.7
0.5
0.6
$
3
- a
.-
CTZ
I
0
0.
II
0.2
I
I
0.3
I
0.4
I
0.I6
0.5
0.7
I
D
Figure 6. Dendrogram of genetic distances ( D ) and identities ( I ) from enzyme electrophoresis data
for the two morphotypes from Paraggi and Zoagli.
presencelabsence data for short and reniform oxeas and strongyles make it
possible to ascribe the cylindrical morphotype to P.Jiciformis and the spherical
one to P. clavata.
The intraspecific spicular variability shown by both species is probably due to
phenotypic plasticity induced by the environment. This variability, which
TABLE
3. Allelic frequencies in the populations of Petrosia from Paraggi and Zoagli
Spherical
Paraggi
GPgd
a
b
N
Mpi
a
N
Hk
a
b
N
Mdh
pg;
10
0.3
0.7
10
I
0
1
10
1
10
1
10
10
0.62
0.38
a
0
1
0.4
0.6
10
1
10
1
10
10
0.8
0
0.2
10
0.2
0.8
0
10
I
0
0
10
LO
a
1
10
1
10
1
10
1
10
a
b
1
0
10
1
0
0
I
10
0
I
10
0
1
10
0
a
x
a
b
x
x
Got
1
10
0
1
10
I
0
10
C
Ak
I
0
10
Cylindrical
Zoagli
0.6
10
N
Es
1
0
10
Cylindrical
Paraggi
0
1
10
a
b
N
TT
Spherical
Zoagli
a
b
x
0.29
0.71
7
0.4
10
0.36
0.64
7
1
1
0
10
1
10
0.6
0.2
0.2
I
10
G . BAVESTRELLO AND M. SARA
58
TABLE
4. Spicular features
P e h s i a jctjormis
Cylindrical morphotype
(from Pulitzer-Finali, 1983)
Spicules
Spicule size
Short and reniform
spicules
Oxeas in part transformed into styles and
strogyles
260 x 12 pm
Always present
Oxeas, styles and strogyles
200-250 x 5- 12 pm
Frequently present
Spherical morphotypr
Petrosia clauata
(from Pulitzer-Finali, 1983)
Spicules
Spicule size
Short and reniform
spicules
Oxeas
140-200 x 4.5-6 pm
Absent
Oxeas and seldom styles
170-200 x 6-8 pm
Absent
may be considered as developmental modulation (Smith-Gill, 1983), is known
for many species of sponges under different environmental conditions such as
water temperature (Hentschel, 1929; Hartman, 1958), water movement
(Palumbi, 1986), silica concentration (Jorgensen, 1944, 1947; Elvin, 1971) and
the annual cycle (Jones, 1987).
The existence of a reproductive barrier between the two forms of Petrosia living
in different zones of the same cave is indicated by the two diagnostic enzyme
loci. This independence could have had its origin in a shift in the reproductive
cycle due to the different environmental conditions in which the two forms live.
Shifts in the reproductive cycle of congeneric species living sympatrically are
known in other Porifera (Siribelli, 1961; Chen, 1977).
A mechanism of parasympatric speciation may be envisaged for the separation
of these two Petrosia species from a common ancestor in relation to the uprise of
new ecological requirements. In the Porifera this mechanism may explain the
frequent occurrence of groups of congeneric species, ecologically distinct, living
in contiguous areas (Sara, 1988).
A typical abiotic factor to which sponge shape is often related is water
movement (Bidder, 1923, 1937; Fry, 1979) which removes the exhaled water
coming from the oscule with its reduced 0, and increased CO, concentrations. If
the water movement is negligible (as it frequently is in dark caves) the sponge is
spherical with one pica1 osculum and its diameter is proportional to the pressure
of the water coming from the osculum in order to prevent its reabsorption
through ostia (Bidder, 1923, 1937). If the water movement is constantly
unidirectional, the sponge is cylindrical with growth only in one direction.
Two hypotheses may be proposed to explain the morphotypes’ speciation. It is
possible that, from a highly variable ancestral species, cylindrical and spherical
mutants were fixed in each habitat by disruptive selection. An alternative
hypothesis takes into consideration the potential ability of an ancestral genotype
to express the two morphotypes via an environmental switch related to water
movement. If the environmental situation was stable the phenotype fixation may
have been accompanied by independent evolution of the newly fixed form which
diverged phenotypically and genotypically from the ancestral group (WestEberhard, 1986, 1989). In our opinion this second hypothesis is more consistent
with the direct relationship of shape of the two species to physical factors.
DIFFERENCES IN POPULATIONS O F PETROSZA
59
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