Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2002
77
Original Article
N. BOUTON
ET AL.
Biological Journal of the Linnean Society, 2002, 77, 185–192. With 1 figure
Experimental evidence for adaptive phenotypic plasticity
in a rock-dwelling cichlid fish from Lake Victoria
NIELS BOUTON*, FRANS WITTE and JACQUES J. M. VAN ALPHEN
Institute of Evolutionary and Ecological Sciences, Leiden University, PO Box 9516, 2300 RA Leiden,
the Netherlands
Received 26 May 2001; revised and accepted for publication 17 May 2002
We demonstrate adaptive phenotypic plasticity (PP) in Neochromis greenwoodi, a rock-dwelling haplochromine
cichlid from Lake Victoria. Adaptive phenotypic plasticity will enhance the chance of survival and reproduction in
changing or novel environments. For rock-dwelling cichlids it may contribute to the success of settlement after
migration between rocky outcrops or islands, since newly colonized patches of rock may offer different food regimes
and different competitors. In our experiments, we simulated such situations by raising fry on different diets and with
different competitors. We chose diet treatments in such a way that we could predict the direction of anatomical
changes from functional demands. We expected an indirect effect of interspecific competition: selectively removing
one prey-type by the competing species would leave N. greenwoodi with the other. We found the predicted phenotypic
responses to food in trophic traits of N. greenwoodi. However, in the current experimental set-up we did not find a
differentiating effect of species of competitor. We discuss the possible role of PP in allopatric and sympatric
speciation. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77, 185−192.
ADDITIONAL KEYWORDS: adaptation − biting-force – feeding − haplochromine − premaxilla − Neochromis
greenwoodi.
INTRODUCTION
Phenotypic plasticity – an environmentally induced
change in the phenotype (Via et al., 1995) – is frequently discussed in relation to speciation (Meyer,
1987; Wimberger, 1991; Day, Pritchard & Schluter,
1994; Robinson & Dukas, 1999; Chapman, Galis &
Shinn, 2000; Losos et al., 2000). Phenotypic plasticity
(PP) may increase the probability of survival and
reproduction in changing or novel environments, perhaps resulting in genetic change through assimilation
(Waddington, 1975; West-Eberhard, 1989). Williams
(1966) argued that such assimilation leads to canalization and thus to an unfavourable loss of flexible
response. However, genetic assimilation can also lead
to a shift in the reaction norm without necessarily
inducing a reduction in PP (Schlichting & Pigliucci,
PLASTICITY IN A CICHLID FROM LAKE VICTORIA
*Corresponding author. Current address: Department of
Oceanography and Fisheries, University of the Azores, Cais
de Santa Cruz, PT-9901–862, Horta, Azores, Portugal.
E-mail: [email protected]
1998). Selection will favour genetic systems that
preserve PP when conditions in the new environment
fluctuate sufficiently (Slatkin & Lande, 1976). Genetic
assimilation that preserves PP will be favourable in
the long term; first, because it preadapts populations
to possible sudden, permanent changes of the environment that resemble some rare environmental condition in the old situation, and second, because it
preserves the possibility for future evolutionary
responses (Schlichting & Pigliucci, 1998).
Rock-dwelling cichlids of Lake Victoria (the study
subject in this paper) may speciate in both allopatry and sympatry at rocky islands and outcrops
(Seehausen & van Alphen, 1999; Bouton, 2000). PP
may contribute to allopatric speciation by helping
individuals to survive and establish populations after
migration between islands. Losos et al. (2000) argue
that PP may have contributed in this way to radiation
of Anolis lizards in the Caribbean. In sympatry, PP
may help to establish resource polymorphisms, a possible first step in sympatric speciation (Kawata, 2002).
Meyer (1987) and Wimberger (1991) discussed the
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77, 185–192
185
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N. BOUTON ET AL.
possible role of PP in cichlid speciation. Meyer (1987)
argued that ‘plasticity may be a form of inertia against
speciation’ in Central American cichlids. In line with
the traditional view that plastic traits evolve slower
than canalized traits (Sultan, 1987) he suggested
that the speciose African cichlids are less plastic.
Wimberger (1991) taking the contrary view, argued
that PP might contribute to speciation in the African
great lakes. There have hitherto been few studies on
PP in cichlids of these lakes (Witte, Barel & van Oijen,
1997), and most of these concentrate on the molluscivore Astatoreochromis alluaudi (e.g. Hoogerhoud,
1986), a lineage that did not speciate in Lake Victoria.
The 100+ species of rock-dwelling haplochromine
cichlids from Lake Victoria are an example of an adaptively radiated group (Seehausen et al., 1998). Rockdwelling haplochromines in East African lakes are
stenotopic; in these species, PP may be a way to deal
with changing local circumstances or with different
circumstances at newly colonized patches of rock.
These patches of rock often have separate populations
(Dorit, 1990; Arnegard et al., 1999), and regularly
offer different food regimes and different competitors
(Bouton, Seehausen & van Alphen, 1997). In the
present study, we investigate phenotypic responses of
a rock-dwelling cichlid to different food-types, either
as such or as mediated by a competing species.
We chose Neochromis greenwoodi Seehausen &
Bouton, 1998 for the investigation of phenotypic plasticity. It has the most generalized feeding pattern
among rock-dwelling cichlids (Bouton, 1999). In our
experiment, N. greenwoodi had to feed in the presence
of a more effective suction feeder, Pundamilia nyererei
(Witte-Maas & Witte, 1985) or more powerful biter,
Neochromis rufocaudalis Seehausen & Bouton, 1998.
These three species coexist at many rocky islands
and outcrops. Their food in nature varies from
predominantly zooplankton and insect larvae in P.
nyererei, to both insect larvae and filamentous algae
in N. greenwoodi, and mainly filamentous algae in
N. rufocaudalis (Bouton et al., 1997). In feeding performance experiments, N. rufocaudalis collected most per
bite of a substitute for algae, on average 2.6 times as
much as P. nyererei; whereas N. greenwoodi collected
1.7 times as much of the substitute as P. nyererei
(Bouton, van Os & Witte, 1998). Feeding on Chaoborus
larvae, P. nyererei proved to have the best suction
capacity, collecting 1.2 larvae per bout, while N.
greenwoodi and N. rufocaudalis collected 1.0 (Bouton
et al., 1998).
In this study we raised N. greenwoodi on zooplankton and the substitute for algae to test if it was able
to improve its anatomy for biting when fed on the
substitute for algae and improve its anatomy for
suction when fed on zooplankton. We also investigated
effects of competition, hypothesizing that each of the
competitors can influence the prey choice of each N.
greenwoodi specimen . This in turn would lead to adaptive responses in trophic traits. We chose the treatments in such a way that we could predict the
direction of change in trophic traits from functional
demands. Variation in these traits was found among
rocky island populations of N. greenwoodi, and correlated with diet (Bouton et al., 1999).
Thus, our aim was to answer the following questions: (1) whether N. greenwoodi shows phenotypic
plasticity in response to different food-types; (2) if
so, whether interspecific competition influences prey
choice, thereby inducing an adaptive phenotypic
response in the competing focal species.
MATERIAL AND METHODS
EXPERIMENTAL SET-UP
Parent stock of N. greenwoodi was collected at Anchor
Island (2°33′20″S, 32°53′5″ W) in the Mwanza Gulf of
Lake Victoria. To keep genetic variation to a minimum, we used only one large brood ( c. 110 individuals)
taken from parents caught in the wild. Haplochromines are female mouth brooders. Larvae start
feeding immediately after their mother releases them,
but they cannot feed on algae until about 2 weeks after
this time (N. Bouton, pers. obs.). Therefore, we used
larvae of this age and randomly divided them between
the aquaria. In the aquaria we raised N. greenwoodi
either apart or in the presence of N. rufocaudalis or
P. nyererei of the same age. Experiments were initiated in March 1993 and lasted 18 months. To avoid
phenotypic effects of digging in sand (Witte, 1984), we
covered the bottoms of the tanks with plastic sheets
instead of sand.
We had three different diet treatments: ‘algae’,
‘zooplankton’, and ‘algae + zooplankton’. Filamentous
algae (naturally growing on rock boulders in Lake Victoria) were replaced by a substitute referred to as
‘algae’ (Bouton et al., 1998). It was a mixture of commercially available frozen spinach, dry flake food, agar
and water. The agar served to fasten the mixture
tightly to porous concrete slabs measuring 8 × 4 cm.
Slabs with the substitute were replaced twice a day
in the tanks. ‘Zooplankton’ consisted of living Daphnia
in spring and summer or frozen cubes of Cyclops or
Daphnia in the other seasons. Once a week, living
Chaoborus larvae were given instead of Cyclops or
Daphnia. Close relatives of all these planktonic species are present in Lake Victoria, their densities varying between locations and seasons (Witte et al., 1995).
Both living and frozen food were kept in buckets on
top of the tanks and inserted into the tanks every
20 min during daytime, using a small pumping unit
with a time switch. The cubes defrosted in the buckets
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77, 185–192
PLASTICITY IN A CICHLID FROM LAKE VICTORIA
and the zooplankton was kept in suspension with an
airstone. With ‘algae + zooplankton’ fish were fed both
food categories. To avoid morphological differences
caused by allometry, we tried to balance the diet treatments in such a way that growth of N. greenwoodi
would be equal. To this end we did a pilot experiment.
To enforce competition, fish were not fed ad libitum;
food was only available during short periods and fish
were feeding constantly in these periods. We stepwise
increased the amount of food (i.e. numbers of slabs
with ‘algae’ and numbers of zooplankton cubes and
estimated amounts of Daphnia and Chaoborus) during
the experiment, taking fish size into account. However, we did not adjust the amount of food between
treatments, i.e. treatment groups lagging behind in
growth did not receive more food.
We investigated PP solely in response to food by
raising N. greenwoodi on either ‘algae’ or ‘zooplankton’
(Table 1: control groups A and B). Control groups
started with 11 individuals. We investigated effects of
food and competition on growth and phenotypic plasticity in competition groups (Table 1: groups C to H).
Groups C to H started with 22 fishes, 11 individuals of
each of two species. Aquaria C to H had about twice
the volume of A and B, and were given a double quantity of food. Each of the six aquaria had N. greenwoodi
and one of the other species competing for either ‘zooplankton’ (aquaria C, D), ‘algae’ (aquaria E, F), or for
‘algae + zooplankton’ (aquaria G, H, Table 1). In
aquaria with a single food-type we expected differences in growth of N. greenwoodi depending on the
187
competing species, i.e. reduced growth if the competitor was better adapted to the food-type than
N. greenwoodi and vice versa. In aquaria with two
food-types we expected the competitors to influence
N. greenwoodi’s prey choice. This could lead to differences in trophic traits depending on the competing
species.
Although we had 11 individuals of N. greenwoodi in
each treatment, the treatments themselves were not
replicated. This was a consequence of the high demand
on space and time of technicians. Thus it can be
argued that tank effects might cause differences
between treatments. To avoid these effects we kept
other factors constant and all aquaria were connected
to one central water-filtering system. Furthermore, we
could formulate predictions on the direction of anatomical changes based on functional morphology (see
below).
The experiments were in compliance with the Dutch
animal health care regulations.
MEASUREMENTS, CALCULATIONS,
AND PREDICTIONS
We used standard length as a measure of size and
calculated its mean for each experimental group
(Table 1). Standard length (SL) is the distance from
the rostral tip of the upper jaw to the origin of the caudal fin (Barel et al., 1977). Following van Leeuwen &
Spoor (1987) we calculated biting force of the lower
jaw as:
Table 1. Design of the phenotypic plasticity experiment using the focal species N. greenwoodi. Column one lists aquarium
and group labels, columns two and three the relative amounts of ‘zooplankton’ (z) and ‘algae’ (a). Column four lists the
competing species (if present) with the number of specimens that survived until the end of the experiment in parentheses.
All groups started with 11 individuals. Nsurv, number of N. greenwoodi that survived until the end of the experiment; M/F,
sex ratio of surviving fishes; M/SL and F/SL, standard length of males and females at the end of the experiment. Each
sex was tested to establish whether SL differs between treatments with the same food-type, or between competing species.
NS, not significant (ANOVA, P > 0.05)
Nsurv
Control groups: 200-L aquaria
A
1z
B
1a
N. gree. only
N. gree. only
Competition groups: 375-L aquaria
C
2z
D
2z
E
F
G
H
1z
1z
M/F
M/SL
F/SL
5
4
1/4
0/4
+ N. rufo. (n = 9)
+ P. nyer. (n = 11)
11
10
5/6
3/7
57.3 ± 2.3
58.7 ± 0.6
NS
53.6 ± 1.6
53.7 ± 2.9
NS
2a
2a
+ N. rufo. (n = 11)
+ P. nyer. (n = 11)
10
10
4/6
3/7
78.2 ± 2.9
78.0 ± 3.3
NS
71.4 ± 2.3
68.4 ± 2.9
NS
1a
1a
+ N. rufo. (n = 9)
+ P. nyer. (n = 6)
7
9
1/6
3/6
76.1
75.9 ± 2.8
NS
67.5 ± 2.2
70.1 ± 3.1
NS
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77, 185–192
188
N. BOUTON ET AL.
Vm
R to Z
R to Z
= c*
*
C to D R to T
R to T
R to Z
1
= c * Vm *
*
C to D R to T
FT = FM *
where FT is the biting force of the lower jaw, FM is the
power that can be exerted by the musculus adductor
mandibulae, calculated as a species-specific constant
(c) times the physiological cross section of the muscle.
The latter is calculated as dry weight (V m) of the muscle divided by fibre length (C to D, Fig. 1A). The constant is omitted in comparisons between treatments,
since it is unlikely to differ within a species. R to Z
denotes the length of the arm from the centre of rotation (R) perpendicular to a muscle fibre to the point
where it crosses this fibre (Z, Fig. 1A), and R to T
denotes the length of the lower jaw from centre of rota-
Figure 1. Anatomical models. A. Biting force of the lower
jaw (after Van Leeuwen & Spoor, 1987). FT, biting force; R
to T, lower jaw length; C to D, muscle fibre length; R to Z,
length of arm perpendicular to muscle fibre. B. The premaxilla. b, the angle between ascending and dentigerous
arms; A to B, length of the ascending arm.
tion (R) to the tip of the most exterior tooth (T,
Fig. 1A). Muscle fibres attach to different points on the
posterior extension of the lower jaw, resulting in various values for fibre length (C to D) and arm (R to Z).
Therefore, we segmented the muscle surface into six
parts and calculated the ratio for each part. The ratio
proved to be approximately constant throughout the
muscle as both arm and fibre length are decreasing
from dorsal to ventral. Thus, we used the average. For
direct comparability FT was divided by the square of
medial head length (mHL), i.e. the length of the perpendicular line in the medial plane in the triangle
formed by the rostral tip of the upper jaw and the most
caudal points of the opercula. We used the square of
mHL, because biting force is proportional to the cross
section of the musculus adductor mandibulae.
We measured two aspects of the premaxilla: the relative length of the ascending arm l/mHL and the angle
b between the ascending and the dentigerous arms
(Fig. 1B, Witte, 1984). For downward suction feeding,
most fish species protrude the premaxilla. Protrusion
will be enhanced if the ascending arm of the premaxilla (l) is long. In contrast, shortening the ascending
arm optimizes transmission of biting force (Otten,
1983). Transmission of biting force is further
enhanced by increasing the angle b (Otten, 1983).
From the functional and morphological point of view, a
high biting force is supposed to be adaptive for fishes
feeding on filamentous algae (Barel, 1983; Norton,
1995) and a long ascending arm of the premaxilla
adaptive for suction feeding. This was confirmed in
feeding experiments on the algae substitute and mosquito larvae (Bouton et al., 1998). Note that trade-offs
between suction feeding and biting exist, because
these modes of feeding impose conflicting demands on
anatomy. We predicted that N. greenwoodi including
(more) ‘algae’ in their diet would differ in the following
ways from those including (more) ‘zooplankton’: (1) the
biting force of the lower jaw would be larger; (2) the
angle b between the arms of the premaxilla would be
larger, and (3) the ascending arm of the premaxilla
would be shorter.
To investigate the effect of food alone on the extent
of (adaptive) phenotypic plasticity we compared the
anatomy between the control groups A and B. To
investigate the effects of competition, food, and the
interaction between the two, we performed a MANOVA
on measures of the six N. greenwoodi groups with the
three diet treatments with one of the two competitors
(N. rufocaudalis or P. nyererei). In addition we used
ANOVA for direct comparison between groups.
RESULTS
The control groups (A and B) could not be used for any
comparisons since mortality, most likely caused by
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77, 185–192
PLASTICITY IN A CICHLID FROM LAKE VICTORIA
aggression of the dominant fishes, was very high
(Table 1). Dominant fishes were seen to chase and bite
others, which eventually sustained damage and died.
In competition groups consisting of 11 individuals of
N. greenwoodi and 11 of another species, aggression
was divided over more individuals, and this prevented
high mortality.
Growth – measured as standard length (SL,
Table 1) at the end of the experiment – did not differ
between groups of the focal species, i.e. groups that
had been raised on the same food-type but with a different competitor. Neochromis greenwoodi raised on
‘algae’ reached the same size when competing with
N. rufocaudalis as with P. nyererei, and the same
holds for the other diet treatments ‘zooplankton’ and
‘algae + zooplankton’ (Table 1). However, growth of
N. greenwoodi differed between diet treatments; the
‘zooplankton’ groups (C and D) remained smaller than
the others and did not overlap in size with those
including algae in their diet ( ANOVA, P < 0.001,
Table 1). We excluded these from the MANOVA that we
performed on measures of trophic traits of all competition groups, because we could not distinguish
between effects of allometric growth and PP. In the
other four groups (E−H) specimens reached similar
average sizes (Table 1). In the MANOVA we did not differentiate between sexes, because trophic traits do not
differ between sexes in these species (Seehausen et al.,
1998). Differences in trophic anatomy between the
‘algae’ and ‘algae + zooplankton’ groups were an effect
of food only (MANOVA, Table 2). No effect was found of
the competing species or of the interaction between
food and competitor (Table 2).
To investigate the effect of food, results of measurements on the anatomy of groups with the same food
(but different competitor) were joined (E + F and
G + H, Table 3). Two out of three anatomical characters (FT/mHL2, b) of N. greenwoodi differed significantly between the treatments ‘algae’ and ‘algae +
zooplankton’. In accordance with predictions from
functional morphology, the algae groups had a larger
Table 2. Results of MANOVA on the three anatomical characters (FT/mHL2, l/mHL, and β ) of the four N. greenwoodi
groups raised with P. nyererei or N. rufocaudalis as a competitor on either ‘algae’ or ‘zooplankton + algae’. See Table 3
for an analysis of the effect of food on anatomy
Test for effect
Wilks’ L
F-value
P
food
competitor
food*competitor
0.756
0.956
0.902
3.34
0.48
1.13
0.032
0.699
0.353
189
biting force and a larger angle b between the arms of
the premaxilla than the ‘algae + zooplankton’ groups.
The length of the ascending arm of the premaxilla did
not differ between these groups.
DISCUSSION
Mortality is a problem in plasticity experiments,
because selective mortality can be an alternative
explanation for observed phenotypic differences
between treatments. In some studies on PP of cichlids,
data on mortality cannot be retrieved, because the
number of individuals at the start of the experiment is
not given (Meyer, 1987; Wimberger, 1991; Chapman
et al., 2000). Except for the control groups and aquarium G, mortality was low in our experiment. Measurements were taken from three specimens (two from
aquarium G, one from F) that died before the end of
the experiment. Premaxilla measures (biting force of
the lower jaw could not be measured due to decay of
the muscle tissue) for each of these specimens were
around their respective group averages, indicating
that mortality was not associated with unfavourable
trophic traits.
A phenotypic response has been demonstrated in
N. greenwoodi; we assume that this is a response to the
food offered. However, it can be argued that some
other factor caused the observed differences, since
individuals with the same treatment were raised
together in the same aquarium (the problem of pseudoreplication). There are two arguments against this
supposition. First, since we did not find food-bycompetitor-species interactions or differential effects
of the competing species, we can independently com-
Table 3. An anatomical comparison between diet treatments: ‘algae’ (A, groups E + F), and ‘algae + zooplankton’
(AZ, groups G + H). Indicated are mean ± SD for standard
length (SL) and three trophic traits: biting force of the
lower jaw (FT/mHL2), length of the ascending arm of the
premaxilla (l/mHL), and angle between the ascending arm
and the dentigerous arm of the premaxilla ( β ). P-values are
based on two way ANOVAs. Values of the ‘zooplankton’ treatments (Z, groups C + D) are given as well, but not used in
any comparison, because of the size difference with the
other groups
SL
FT/mHL2
(·105)
l/mHL
(·102)
b
A (n = 20)
AZ (n = 16)
P (A–Z)
Z (n = 21)
72.7 ± 5.0
55.4 ± 5.6
70.6 ± 4.2
50.5 ± 8.1
NS
<0.05
55.3 ± 3.0
43.0 ± 6.6
26.7 ± 1.5
27.2 ± 0.9
NS
27.2 ± 1.2
93.4 ± 2.4
89.0 ± 1.6
<0.001
91.5 ± 2.4
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77, 185–192
190
N. BOUTON ET AL.
pare traits of N. greenwoodi of groups E (‘algae’ +
N. rufocaudalis) and F (‘algae’ + P. nyererei) with those
of group G (‘algae + zooplankton’ + N. rufocaudalis)
and H (‘algae + zooplankton’ + P. nyererei). This yields
four possible tests (E-G, E-H, F-G, F-H) that we compiled with a Bonferroni procedure. The angle b of the
premaxilla was significantly larger (ANOVA, P < 0.01)
in the ‘algae’ groups than in the ‘algae + zooplankton’
groups. The within-group variance in biting force of
the lower jaw is rather large, possibly because of the
complexity of the measurements. This measure did
not differ in any of the four comparisons ( ANOVA,
P > 0.05); the symmetry of results (significant differences in b, non-significant differences in biting force)
supports the interpretation that there were no aquarium effects. Second, we formulated expectations about
the direction of differences between treatments. We
used food-types that imposed contrasting demands on
the anatomy of the jaws and found differences in two
out of three jaw characters for each of the groups that
matched the predictions, viz. a larger biting force of
the lower jaw and a wider angle b between ascending
and dentigerous arms of the premaxilla in the group
raised on ‘algae’. The most plausible explanation is
that food and the required feeding techniques caused
the differences in trophic traits. Similar observations
were made in Harpagochromis squamipinnis from
Lake George and in the Central American Herichthys
minckleyi, where, respectively, b and snout acuteness
(encompassing b) increased when raised on food types
that demanded biting (Witte, 1984; Meyer, 1987).
While we did find an adaptive response to food, we
did not find an effect of the species competing with
N. greenwoodi. We supposed that the more powerful
biter would collect more ‘algae’ and the more effective
suction feeder more ‘zooplankton’. This could result
in: (1) dependence of growth of N. greenwoodi on the
competing species (in aquaria with a single food-type)
or (2) dependence of diet and trophic traits of
N. greenwoodi on the competing species (in aquaria
with two food-types, one would be removed efficiently
by the competing species). Growth differences were
not found (Table 1), and neither were anatomical differences in response to competition (Table 2). There
are two possible explanations. First, interspecific competition for food occurs in the lake, but could not be
traced in the experiment. The reason for this might be
that constant but low food levels prevail in the lake
(Bouton et al., 1997), while in the experiment, periods
without food alternate with short periods of high food
abundance. Second, the lack of interspecific competition for food in the experiment reflects that in the lake.
The diet of N. greenwoodi at different rocky islands
indeed seems more determined by the resource base
than by the presence of competitors. At Python Island
N. greenwoodi includes more nonattached organisms
in its diet than at Anchor Island, despite the presence
of large numbers of competitors that feed predominantly on these organisms at the former island (Bouton et al., 1999).
Field observations on N. greenwoodi were the starting point for this experiment. Populations living
around different rocky islands exhibit differences in
diet similar to treatments in the experiment. For
example, the population of Anchor Island had a higher
proportion of attached organisms (41%) in its diet
than that of Python Island (22%, Bouton et al., 1999).
Between these populations, we found differences in
anatomy that were in concordance with predictions
from functional morphology based on the diet (Bouton
et al., 1999). However, these differences were not
exactly the same as in the experiment. Between the
populations of the two islands, both the angle b and
the length of the ascending arm of the premaxilla differed, but not the biting force of the lower jaw.
Between the experimental groups, the biting force of
the lower jaw and the angle b of the premaxilla differed, but not the length of the ascending arm. Thus in
the field adaptive changes favouring suction feeding
prevail (in the population of Python Island), while in
the experiment adaptive changes favouring biting prevail (in the ‘algae’ group). This may be explained by
the fact that the Python Island population and the
‘algae’ group had the most extreme diets. The Python
Island population had 78% nonattached organisms
(requiring suction feeding) and 22% attached organisms (requiring biting), while the ‘algae’ group had
100% attached organisms (requiring biting). The
Anchor Island population (41% nonattached, 59%
attached) and the ‘algae + zooplankton’ treatment
(50% nonattached, 50% attached) had more balanced
diets. Thus, adaptive changes may be invoked by more
extreme diets.
Plastic responses may be deleterious for surrounding structures. Chapman et al. (2000) found a 29%
larger gill surface in a haplochromine from a low oxygen site (in the swamps surrounding a small lake in
the Lake Victoria basin) compared to one from a high
oxygen site (in the small lake itself). Further, they
found in plasticity experiments that individuals raised
in low oxygen conditions also developed a larger gill
surface. However, the plastic response (longer filaments and larger secondary lamellae) differed partly
from the long-term response that was observed in the
field (more and longer gill filaments). The plastic
response seemed to have a stronger trade-off with
feeding performance. Thus, Chapman et al. (2000) concluded that plastic responses might interfere with
other functions, while long-term selection might neutralize these detrimental effects. In our experiment, a
higher biting force of the lower jaw was achieved by
enlarging the adductor muscle (N. Bouton, pers. obs.).
© 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77, 185–192
PLASTICITY IN A CICHLID FROM LAKE VICTORIA
The enlarged claim on space of this muscle may have
detrimental effects on functions such as suction feeding and respiration, and on streamlining (Barel,
1993). Therefore, long-term selection may favour other
ways to achieve a higher biting force. Powerful biters
(such as N. rufocaudalis) are distinguished by a
favourable lever arm on the lower jaw rather than by
a large adductor muscle (N. Bouton, pers. obs.).
Plasticity may add to the opportunities for settlement and local adaptation in N. greenwoodi after
migration. Long-term selection and possibly genetic
assimilation of plastic traits may drive the populations further apart and may ultimately result in
allopatric speciation. Theoretical approaches show
that similar ecological divergence is possible in sympatry if, for instance, an unexploited food source is
available in the habitat (Dieckmann & Doebeli, 1999;
Kawata, 2002). PP may help to establish a resource
polymorphism in that situation. The chance of subsequent speciation depends on the size of the genetic
neighbourhood (Kawata, 2002). Since haplochromine
cichlids lack premating migration and larval dispersal, they typically have a small genetic neighbourhood. This enhances the chance of sympatric
speciation. Thus, rock-dwelling haplochromines are
good candidates for both allopatric and sympatric speciation driven by ecological interactions, and PP may
play a key role in the initiation of speciation processes.
ACKNOWLEDGEMENTS
We thank P. Snelderwaard for his practical support
during the experiment and S. Zeilstra for helping with
administration of the specimens. J. Dubbeldam, P.
Haccou, L. Kaufman, O. Seehausen, and two anonymous referees are thanked for valuable comments on
earlier drafts of the manuscript. Our colleagues of the
Tanzania Fisheries Research Institute (TAFIRI) are
thanked for their hospitality. M. Richardson improved
the English. M. Brittijn drew the figure. The research
was supported by WOTRO-grant W84-282.
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