Anim. Behav., 1995, 49, 377–387
Offspring quality and female choice in the guppy, Poecilia reticulata
PAUL F. NICOLETTO*
Department of Biology, University of New Mexico, Albuquerque, NM 87131, U.S.A.
(Received 7 September 1993; initial acceptance 21 October 1993;
final acceptance 24 January 1994; MS. number: 6624)
Abstract. This study evaluated the offspring viability prediction of the condition-dependent and
Fisherian models of female choice in the guppy. Families of full-sibling females were bred with the male
they preferred or did not prefer in a choice experiment. The physical condition, sexual behaviour and
coloration of the offspring were evaluated. There were no significant differences between offspring
attributable to the type of sire. However, there were significant family and sire-type by family
interactions for physical condition, male mating behaviour and coloration. These significant effects
indicate that consistency within families may be due to genetic effects. Genetic analyses indicate that
genetic variation probably exists for prolonged swimming performance, physical condition and display
rate. The results of this study and other studies on other fish have shown that these measures of
constitution are correlated with components of viability. These results are interpreted in the framework
of the condition-dependent and Fisherian models of female choice.
The Fisherian and condition-dependent models of
female choice are often cited to explain the evolution of elaborate male ornamentation in species
without male parental care. The Fisherian model
contends that male ornaments evolve because
females have a genetically based mating preference for certain male traits. Male traits are arbitrary. The only advantage a female receives from
her preference is the production of ornamented
sons which will have greater mating success in the
next generation (Lande 1981; Kirkpatrick 1982,
1987; Heisler et al. 1987). The conditiondependent model contends that females use the
development of male ornaments as indicators of
genetic quality (Zahavi 1975; Andersson 1982,
1986; Hamilton & Zuk 1982; Kodric-Brown &
Brown 1984; Nur & Hasson 1984; Pomiankowski
1987a, b, 1988). Male advertising traits provide females information about the male’s ability
to exploit the current environment. Females
indirectly enhance their fitness by producing
high-quality female and male offspring.
Learning which of these models best explains
the evolution of male ornamentation has been
problematic, because the two models make many
similar predictions (Heisler et al. 1987; Balmford
& Read 1991; Kirkpatrick & Ryan 1991). How*Present address: Department of Biology, Shippensburg
University, Shippensburg, PA 17257, U.S.A.
0003–3472/95/020377+11 $08.00/0
?
ever, they do differ with respect to the relationship
between a female’s choice of a mate and the
viability or fitness of her offspring (Heisler et al.
1987; Balmford & Read 1991; but see Nicoletto
1993). The Fisherian hypothesis predicts that
there is no relationship between female choice and
offspring fitness. The condition-dependent model
predicts that there is a positive relationship
between female choice and offspring fitness
(Zahavi 1975; Kodric-Brown & Brown 1984;
Heisler et al. 1987).
Viability is used in the genetic models of
Fisherian and condition-dependent female choice
as a measure of offspring quality (Anderson 1982;
Arnold 1985; Maynard Smith 1985; Kirkpatrick
1987). Because of logistical contraints on the
researcher, however, and the limitations imposed
by an organism’s life history most empirical
studies of female choice have been unable to
measure offspring viability directly (but see
Partridge 1980; Boake 1989). Most researchers use
variables that are related to an animal’s phenotypic condition or constitution, for example
swimming performance (Nicoletto 1991, 1993),
condition factor (Andersson 1989; Milinski &
Bakker 1990; Nicoletto 1993) and parasite resistance (Kennedy et al. 1987; Ligon et al. 1990; Zuk
et al. 1990; Houde & Torio 1992) because they are
components or correlates of overall viability. Constitution is defined as ‘the physical makeup of the
1995 The Association for the Study of Animal Behaviour
377
Animal Behaviour, 49, 2
378
individual comprising inherited qualities modified
by environment’ (Webster’s New Collegiate Dictionary 1981). I will use constitution as a general
term for components or correlates of viability
such as those mentioned above.
The objective of this study was to evaluate the
relationship between female choice and offspring
viability in the guppy. I tested the prediction that
there is a significant difference in constitution
between offspring of females mated to preferred
males and offspring of females mated to nonpreferred males.
Guppies are particularly appropriate to study
because females use a variety of male characteristics during mate choice and some of these characteristics are condition-dependent. Females
respond to males on display rate (Farr 1980;
Houde 1988), colour pattern (Endler 1980, 1983;
Kodric-Brown 1985, 1989; Houde 1987, 1988;
Long & Houde 1989; Houde & Endler 1990),
dorsal and caudal fin size and shape (Bischoff
et al. 1985), and colour intensity (Kodric-Brown
1989; Houde & Torio 1992). Male display rate,
area and intensity of orange coloration, and overall ornament complexity are positively correlated
to prolonged swimming performance in males
(Nicoletto 1991, 1993). Display rate is also correlated with male physical condition (Nicoletto
1993) and negatively correlated with parasite load
(Kennedy et al. 1987; McMinn 1990).
MATERIALS AND METHODS
Female Choice Experiment
I conducted a female choice experiment to
choose sires for a breeding experiment. Each
laboratory-reared female was presented with four
males, simultaneously, which were size-matched
(within 2 mm), had individually recognizable
colour patterns, and had dorsal and caudal fins of
similar size and shape.
Female choice trials were performed in an
aquarium measuring 50#50#20 cm with a central compartment (20#20#20 cm) for the female
and four peripheral compartments for the males.
The four male compartments were made by placing opaque partitions from the corners of the
choice tank to the corners of the female compartment at a 45) angle. This aquarium had an undergravel filter, and a dirty white coral substrate.
Each male compartment contained a submersible
heater. The water temperature in each compartment ranged between 27 and 29)C. A mirror
(60#60 cm) was placed 0·66 m above the tank at
a slight angle to enable simultaneous observation
of all compartments. A VHS camcorder placed on
the floor in front of the tank was focused on the
mirror and used to record the experiment.
Four males and a single female were allowed to
acclimatize to the choice aquarium for 24 h before
the female choice trial. Opaque partitions, similar
to those separating males, were placed around the
central female compartment before the choice
experiment and prevented the female from seeing
the males. These partitions were removed at the
beginning of the experiment. Each female’s choice
of a male was determined by filming the female for
a 25-min observation period. Data were not
recorded for the first 5 min to reduce the effects of
disturbance caused by removing the partitions. I
ranked males based on how much time the female
spent within 2 cm of the male’s partition during
the 20-min observation period. The male with
which a female spent the most time was recorded
as a positive choice (preferred male). The male
with which a female spent the least time was
recorded as a negative choice (non-preferred
male). The female was then mated to the least
preferred or most preferred male. Each guppy was
only used once in this experiment. Male display
rate was not recorded because the displays could
not reliably be detected on the television screen.
All choice experiments took place between 0800
and 1000 hours in a greenhouse under natural
light.
I collected the males used in the female choice
experiment from a feral population in McCauley
Hot Spring in the Jemez Mountains of New
Mexico (see Nicoletto 1993). I captured males at
approximately monthly intervals and allowed
them to acclimatize to laboratory conditions for
at least 2 weeks before testing.
The females I used in the choice and breeding
experiment were from a third-generation laboratory colony derived from the Jemez Mountain
population. All of the females used in the female
choice and breeding experiments were virgins
reared without males present in their aquarium. I
raised 16 families of females and arbitrarily chose
six females (full-siblings) from each family, for a
total of 96 females. Each of these females was used
as a dam in the breeding experiment. A ‘damfamily’ consisted of all six females from one
Nicoletto: Offspring quality and female choice in guppies
family, thus there were 16 dam-families each containing six full-siblings. The use of sets of
laboratory-reared sisters minimized phenotypic
and genotypic variation within a family of females
because they were full-siblings and reared in
constant conditions.
Breeding Experiment
I designed a breeding experiment to determine
whether there were any significant differences
between the offspring of females mated with their
preferred male versus the offspring of females
mated to their non-preferred male. Three sisters in
each family were mated with the males they
preferred during their female choice experiment.
The other three sisters in each family were mated
to the males they did not prefer during their
female choice experiment.
I used 42-litre aquaria that were divided in half
as breeding and rearing tanks. Each tank contained a single preferred pair and a single nonpreferred pair from the same dam-family. Each of
these tanks contained an undergravel filter that
allowed water to circulate between the two compartments. A plastic or glass aquarium lid was
placed over the aquarium to prevent fish from
jumping between compartments. A submersible
heater was placed next to the partition dividing
the aquarium. The water temperature was kept
at 28)C and differed by less than 2)C on either
side of the partition. A floating plastic plant
in each compartment provided a refuge for
offspring.
Sires remained with the dams for at least 20
days to ensure insemination. The female remained
with the brood and often had multiple litters.
These litters were not separated or counted.
Within 2 weeks after the first male offspring
reached sexual maturity, as determined by male
gonopodial and colour development, I arbitrarily
chose two males and two females from each litter.
These fish were housed individually in one of
four compartments of a 42-litre aquarium and
were visually isolated. All fish were fed Tetramin
tropical fish food at least twice daily and were fed
brine shrimp approximately every other day. I
measured the swimming performance and calculated a condition factor for each male and female
offspring (see below). I also photographed male
offspring and used them in a female sexual
response experiment as described below.
379
Prolonged Swimming Performance
I determined the prolonged swimming performance of the parents and offspring by measuring
critical swimming speed. Critical swimming speed
is the maximum speed that a fish can sustain for a
set period in a laboratory flow chamber (Brett
1964). Critical swimming speed is a common
measure of prolonged swimming performance
and reportedly correlates well with health, active
metabolism and endurance in other fish species
(Brett 1964; Smit 1965; Brett & Glass 1973; Jones
et al. 1974; Beamish 1978). I measured critical
swimming speed by increasing the water velocity
in the flow chamber every 3 min until the fish
became exhausted. A description of the flow
chamber and the methodology for measuring
swimming speed are given in Nicoletto (1991,
1993).
Condition Factor
The physical condition of parents and offspring
was estimated by calculating a condition factor.
Condition factors are used to estimate the relative
physical condition or ‘stoutness’ of fish (Bolger &
Connolly 1989; Milinski & Bakker 1990). These
factors assume that, at a given standard length,
heavier fish are in better physical condition. I
calculated the equation for the condition factor
separately for the field-caught male parents (Fig.
1) and laboratory-reared female parents and all
offspring (Fig. 2). Standard lengths of all fish were
measured with dial calipers to the nearest
0·01 mm. Mass was measured to the nearest
0·001 g with an electronic balance. The equation
for the condition factor was calculated as
Condition=Mass(g) #100/(Length(cm)b), where b
is equal to the slope. The slope was calculated by
fitting a multiplicative regression model to the
relationship between mass and standard length
(Figs 1, 2).
Colour Quantification
I measured the colour patterns of male parents
and offspring by projecting a colour slide of each
fish on a computer digitizing tablet. Details of the
photography and measurement procedures are
given in Nicoletto (1993). The proportion of the
fish’s body that was covered by each colour was
used in the analysis to correct for differences in
body size. I used ornament complexity (the area
380
Animal Behaviour, 49, 2
two separate sets of rankings, one set for males
from the female choice experiment and one set for
the male offspring. The number of structural spots
was not included in this analysis because these
spots are usually continuously distributed on a
male’s body.
Female Sexual Response to Male Offspring
Figure 1. The relationship between standard length
and mass for field-caught sires used in the breeding
experiment.
This experiment used a no-choice design to
evaluate the attractiveness of male offspring and
all sires to females. In a no-choice design, females
are presented a single male and are not given a
choice between different males. The details of this
experiment are given in Nicoletto (1993). This
experiment consisted of presenting each male with
a virgin female and recording the male’s display
behaviour and female’s sexual response (Liley
1966; Houde 1987, 1988; Reynolds & Gross 1992).
Virgin females were obtained from a stock
aquarium and were not the daughters or siblings
of the males. The variables recorded during each
3-min observation period were: number of male
displays, copulatory attempts, and the number of
female sexual responses. A female sexual response
was counted when the female oriented towards the
male and either glided or slowly swam towards
him (Houde 1987, 1988). These female behaviour
patterns indicate that the female is receptive to the
male’s advances and are related to male mating
success (Liley 1966; Houde 1987, 1988). This
experiment took place in aquaria under full spectrum Vita lights placed 6·25 cm above the
aquarium. I evaluated the female sexual response
for the 107 male offspring and 96 sires from the
breeding experiment.
Statistical Analysis
Figure 2. The relationship between standard length and
mass for laboratory-reared dams and their mature male
and female offspring that were used in the breeding
experiment.
and number of orange and black colour spots and
the area of structural colours) to quantify ornamentation. Ornament complexity was calculated
by ranking each colour variable separately and
then summing the ranks for each colour for each
male. Therefore, ornament complexity is a variable that ranks the complexity of a male’s total
ornamentation relative to others in the sample
from which it came (Nicoletto 1993). I performed
The characteristics of preferred and nonpreferred males (N=192) of individual females
from the female choice experiment were analysed
using Wilcoxon matched-pairs signed-ranks tests.
The characteristics of preferred and non-preferred
sires (N=96) used in the breeding experiment were
compared using Wilcoxon rank-sum tests. These
analyses test the hypothesis that the constitution
and ornamentation of preferred males is greater
than that of non-preferred males, thus the
P-values resulting from these analyses are onesided. The one-sided tests are justified because
both the Fisherian and condition-dependent
models of female choice predict that females will
Nicoletto: Offspring quality and female choice in guppies
choose males with the best developed ornamentation, and the condition-dependent model predicts
that these males will also be in the best physical
condition (Heisler et al. 1987).
All data collected on the offspring from the
breeding experiment were analysed using a 2#2
factorial analysis of variance (ANOVA). The
effects or treatments in the model were the sire
type (i.e. either a preferred or non-preferred),
dam-family and the interaction between sire type
and dam-family. Male and female offspring were
combined for the critical swimming speed and
condition-factor analyses. The critical swimming
speed and condition factors of male and
female offspring were not significantly different
(Wilcoxon rank-sums test, P=0·402 and 0·978,
respectively). Therefore, I did not use sex as a
main effect in these analyses. Critical swimming
speed and the condition factor were normally
distributed. The ornament data and the female
response data were rank transformed (Conover &
Iman 1981) and the ranks were analysed in the
ANOVAs on these variables. The P-values for the
overall F-test for each ANOVA were sequentially
Bonferroni adjusted to protect against type 1
error. The P-values within each ANOVA were not
adjusted.
There were different sample sizes for the various
ANOVAs, because 14 mated pairs failed to produce offspring. Therefore the data set was unbalanced and analysed with PROC GLM (SAS
1988). Eight of these pairs were preferred matings
and six were non-preferred. Some additional pairs
failed to produce the required four offspring. In
addition, the female response experiment was only
performed on 15 families of offspring.
The ANOVAs revealed significant dam-family
effects that were probably due to genetic variation
and not environmental variation. Genetic variation is important because the condition-dependent
model of female choice contends that ornament
development is correlated with components of
male constitution that can be passed on to offspring (Zahavi 1975; Kodric-Brown & Brown
1984; Heisler et al. 1987). Thus, there must be
heritable genetic variation in the components of
constitution that are correlated with the development of a male’s ornamentation. Therefore, I
performed quantitative genetic analyses to determine whether they would also support the genetic
interpretation of the ANOVAs. Because this study
was not designed to measure heritability, the
381
heritability values reported here are either broadsense heritabilities or biased estimates of narrowsense heritabilities. Broad-sense heritability is an
estimate of the total phenotypic variation in a
character that is due to all genetic factors, that is,
additive, dominance, epistatic and maternal variance components (Becker 1984). Narrow-sense
heritability is an estimate of the total phenotypic
variation in a character that is due to additive
variance components (Becker 1984; Falconer
1989).
The broad-sense heritability of critical swimming speed and the condition factor were estimated by using the methodology described by
Becker (1984, pp. 52–57) for single pair matings.
This analysis is appropriate when pairs of individuals are chosen randomly from a population
and mated together and each mated pair produces
several offspring. This is how the 16 dam-families
consisting of six full-sisters (dams in the sire-type
breeding experiment) were obtained.
The narrow-sense heritability analyses for the
constitution, ornaments and female response variables were done with mean parent offspring
regressions (Becker 1984; Falconer 1989). The
narrow-sense heritability estimates for the sire–
son and sire–daughter regressions should be interpreted with caution because the sires were fieldcaught and the offspring were laboratory reared.
Dam–son and dam–daughter heritability estimates may contain additive and maternal components because guppies are live bearing, and
maternal effects have been demonstrated for offspring growth rate and mass (Rocchetta et al.
1985).
RESULTS
Female Choice Experiment
In the female choice experiment, differences
between preferred and non-preferred males in
critical swimming speed, ornament complexity
and black area tended towards significance. The
ornament complexity and orange number of the
sires also tended towards significance. However,
there were no significant differences in any of
these variables after a sequential Bonferroni
adjustment (Tables I and II).
Breeding Experiment
The breeding experiment tested the prediction that there was a significant difference in
Animal Behaviour, 49, 2
382
Table I. Wilcoxon matched-pairs signed-rank test on the results of the mate choice
experiment
Average rank
Variable
Preferred
Non-preferred
z-statistic
P-value
Critical swimming speed
Condition factor
Ornament complexity
Orange area
Black area
Structural area
Orange number
Black number
102·6
94·8
102·7
100·4
105·7
96·9
98
95·9
90·4
98·1
91·3
92·6
87·3
96·1
94·9
97·01
"1·528
0·401
"1·416
"0·966
"2·304
"0·103
"0·386
0·131
0·063
0·344
0·075
0·167
0·011
0·559
0·345
0·445
Note that no P-value was statistically significant after a sequential Bonferroni
adjustment.
Table II. The results of Wilcoxon rank-sums tests on the males used as sires in the
breeding experiment
Average rank
Variable
Preferred
Non-preferred
z-statistic
P-value
Critical swimming speed
Condition factor
Ornament complexity
Orange area
Black area
Structural area
Orange number
Black number
51·7
45·7
52·9
50·7
51·9
49·5
54·1
51·1
46·3
51·3
47·9
46·3
45·1
47·5
41·8
44·9
"0·949
0·971
"1·753
"0·77
"1·21
"0·337
"2·198
"1·107
0·171
0·165
0·039
0·221
0·111
0·365
0·013
0·131
Note that no P-value was statistically significant after a sequential Bonferroni
adjustment.
constitution, ornamentation and sexual behaviour
between the offspring of preferred males and
non-preferred males. The ANOVAs on all of the
variables failed to support this prediction, as there
were no significant sire-type effects (Table III).
However, there was a significant dam-family effect
for critical swimming speed, condition factor,
ornament complexity, black area, structural area,
orange number and copulation attempts. The
dam-family effect for display number was marginally significant. The significant dam-family effect
suggests that members of a family tended to be
more similar to each other than to another family.
There were also significant sire-type by damfamily interactions for the condition factor, ornament complexity, black area, orange number and
copulation attempts. The significant interaction
indicates that for some variables the differences
observed in the offspring were attributable to
differences between families and differences
between sire type. This means that in some cases
there are sire-type effects in the next generation
but that this effect is not consistent. The overall
F-tests for the orange area, black number and
female response ANOVAs were not significant
(Table III).
The quantitative genetic analyses tend to support the genetic interpretation of the ANOVAs
(Table IV). The broad-sense estimates for both
critical swimming speed and the condition factor
were greater than zero. The narrow-sense heritability analyses for critical swimming speed, display
number and the female sexual response all yielded
narrow-sense heritability estimates that were
greater than zero (Table V). The narrow-sense
heritability analyses for the condition factor,
Nicoletto: Offspring quality and female choice in guppies
383
Table III. The results of the two-way ANOVAs on offspring from the breeding
experiment
Overall
Variable
F-value
P-value
Source
F-value
P-value
Critical swimming speed
1·78
0·008*
Condition factor
2·37
0·0001*
Ornament complexity
2·23
0·001*
Structural area
1·81
0·013*
Orange number
1·99
0·0005*
Black number
1·15
0·29
Display rate
1·79
0·029
Copulation attempts
2·36
0·002*
Sire type
Dam-family
Interaction
Sire type
Dam-family
Interaction
Sire type
Dam-family
Interaction
Sire type
Dam-family
Interaction
Sire type
Dam-family
Interaction
Sire type
Dam-family
Interaction
Sire type
Dam-family
Interaction
Sire type
Dam-family
Interaction
1·1
2·55
1·15
0·78
1·84
2·82
0·08
2·34
2·15
2·49
2·07
1·32
0·2
1·99
2·2
0·28
1·24
1·15
1·61
1·81
1·63
0·02
3·12
2·01
0·29
0·001
0·31
0·38
0·029
0·0004
0·77
0·006
0·012
0·12
0·016
0·2
0·66
0·021
0·009
0·59
0·25
0·32
0·21
0·06
0·11
0·9
0·001
0·04
*P<0·05 with a sequential Bonferroni adjustment.
Table IV. The results of one-way ANOVAs to determine the genetic variance of guppies
from the dam-families
Source
Dam-family
Variable
Critical swimming speed
Condition factor
N family
N dams
VG

16
16
96
93
0·24
0·71
0·187
0·245
VG: Heritability in the broad sense that contains variance components due to additive,
dominance, epistatic and maternal factors.
copulation attempts and the ornament variables
were not significant. Thus, genetic variation
apparently exists in both critical swimming speed
and some sexual behaviour, but how much of this
variation may be additive is uncertain.
DISCUSSION
The objective of this study was to determine
whether offspring sired by preferred males differed
from offspring of non-preferred males in their
constitution, ornamentation and sexual behaviour. There was no significant difference between
offspring of preferred and non-preferred sires for
any constitution variable that I measured in this
study. This result conforms best to the prediction
of the Fisherian models of female choice. The
Fisherian hypothesis predicts that there is no
relationship between a female’s choice of a mate
and the constitution of her offspring. The significant interaction between sire type and dam-family
Animal Behaviour, 49, 2
384
Table V. The results of parent–offspring regressions
Variable
Critical swimming speed
Condition factor
Display number
Copulation attempts
Female response
Orange area
Black area
Structural area
Potential variance
components
Regression
h2

VA +VE
VA +VE
VA +VM
VA +VM
VA +VM +VE
VA +VE
VA +VE
VA +VM
VA +VM
VA +VM +VE
VA +VE
VA +VE
VA +VE
VA +VE
VA +VE
VA +VE
Sire*son
Sire*daughter
Dam*son
Dam*daughter
Mean
Sire*son
Sire*daughter
Dam*son
Dam*daughter
Mean
Sire*son
Sire*son
Sire*son
Sire*son
Sire*son
Sire*son
0·47
0·09
0·05
0·39
0·25
"0·01
0·13
0·19
0·28
0·15
0·64
"0·12
0·43
"0·02
0·05
0·01
0·132*
0·163
0·150
0·164*
0·152*
0·100
0·102
0·150
0·150
0·130
0·114*
0·228
0·229
0·113
0·064
0·052
VA: Variance due to additive genetic effects; VM: variance due to maternal genetic
effects; VE: variance due to environmental effects.
*Indicates heritabilities that were significantly greater (P<0·05) than zero.
is consistent with this prediction. In some cases,
matings with preferred males resulted in offspring
with better constitutions and more ornamentation, and in other cases, matings with nonpreferred males yielded the same result. In other
words, the lack of a consistent relationship (positive or negative) at the individual level between
female choice and constitution yields no relationship at the population level. However, the
interaction shows that sire type and therefore
female preferences can have an effect in the next
generation.
The results of the analyses of the female choice
experiment revealed no differences in the constitution and ornamentation of preferred and nonpreferred males or sires. Thus, females may have
been choosing males randomly and therefore the
lack of differences between the offspring would be
expected. However, we cannot eliminate the possibility that females were choosing males because
several variables tended towards statistical significance and females could have been choosing
males based upon some unmeasured characteristic. In the Jemez Mountain population, display
rate is probably the proximal cue that females use
to choose males (Nicoletto 1993). I was unable to
measure display rate during the female choice
experiment so there is a possibility that females
were using display behaviour to choose males.
The lack of differences between offspring of
preferred and non-preferred sires in this breeding
experiment are consistent with two unpublished
studies of guppies by A. Houde & A. Gong (J. A.
Endler & A. Gong, personal communication).
These studies found similar results with different
experimental designs. However, Reynolds &
Gross (1992) found that female preferences
based on body size in guppies led to larger offspring size, faster growth rates and higher female
fecundity.
The lack of differences between offspring of
different sire types does not mean that the
condition-dependent model can be dismissed in
this study. Research on guppies has shown that
females use display rate (Farr 1980; Nicoletto
1993), orange ornamentation (Endler 1980, 1983;
Kodric-Brown 1985, 1989; Houde 1988; Long &
Houde 1989) and ornament complexity (Endler
1980, 1983; Nicoletto 1993) during mate choice.
Many of these ornaments are conditiondependent as measured by prolonged swimming
performance, the condition factor (Nicoletto
1993) and parasite load (Kennedy et al. 1987;
McMinn 1990; Houde & Torio 1992). In addition
female guppies respond sexually significantly
more often to males in better physical condition
(Nicoletto 1993) and this sexual response is correlated with mating success (Liley 1966; Houde
Nicoletto: Offspring quality and female choice in guppies
1987, 1988). I have shown that genetic variation
probably exists for prolonged swimming performance and physical condition. However, how
much of this variation is additive remains a question. Studies on other fish species have shown that
prolonged swimming ability and the condition
factor are both correlated with survival components of fitness (Webb 1975; Beamish 1978;
Wootton et al. 1978; Booth & Keast 1986; Bolger
& Connolly 1989). Thus the potential seems to
exist for the condition-dependent model to have
an effect in the next generation.
It seems that all the requirements exist for
condition-dependent female choice to select for
elaborate ornamentation. If this is the case, than
what explains the lack of differences between the
offspring of the different sire types? There are at
least three possible reasons for the lack of differences between offspring. First, there were no differences between offspring of different sire types
because the sires did not differ. Second, this
experiment took place over one generation. The
Reynolds & Gross (1992) study took place over
three generations. Thus, the relationships between
ornamentation and constitution reported elsewhere (Kennedy et al. 1987; Kodric-Brown 1989;
McMinn 1990; Nicoletto 1991, 1993; Houde &
Torio 1992) may not have been large enough to
yield significant differences between offspring
given the sample sizes of this study.
Third, condition-dependent ornaments are
thought to reflect a male’s ability to survive and
procure resources in the habitat and conditions
under which it was born or has lived for a time
(Zahavi 1977; Kodric-Brown & Brown 1984;
Andersson 1986; Zeh & Zeh 1988). Guppy ornamentation, particularly ornament complexity,
orange colour and display rate, are probably
condition-dependent (Endler 1980, 1983; KodricBrown 1989; Nicoletto 1991, 1993; Houde &
Torio 1992). For simplicity I am calling male
display rate an ornament, because it probably
functions to attract the female’s attention.
Females choosing males based on conditiondependent ornaments are potentially evaluating
information about the environment in which
those males live.
Offspring reared in the laboratory encountered
different environmental conditions from their
field-caught sires. A laboratory environment, with
its abundant food and constant conditions, may
have permitted the expression of ornaments in
385
male offspring that were present, but not
expressed, in field-caught sires. It is also possible
that the laboratory environment in this study may
have been good enough that all the offspring of all
the sires had robust constitutions. In either case,
the potential information contained in the sire’s
ornaments did not reflect laboratory conditions
that the offspring were going to encounter. If the
offspring had been reared in the same environment as the sires, differences may have been
observed. In other words, in the laboratory
environment we may find an uncoupling of ornamentation and constitution, so differences in the
ornamentation of offspring of different sire types
were not observed. The uncoupling argument may
also explain why the offspring of preferred males
were not more ornamented than the offspring of
non-preferred males as both the Fisherian and
adaptive models predict.
There are two lines of evidence that support
the idea of uncoupling of ornamentation, orange
colour in particular, and constitution. The relative
area of orange spots in guppies has Y-linked
inheritance and high heritability (Houde 1992) but
the phenotypic expression of orange is affected by
diet (Endler 1980, 1983; Kodric-Brown 1989) and
by parasite load (Kennedy et al. 1987; McMinn
1990; Houde & Torio 1992). In this study, the
field-caught sires had significantly fewer orange
spots with less relative area than their laboratoryreared sons (Wilcoxon matched-pairs signedranks test, comparing the value of the sires with
the average value of the two male offspring,
N=81, orange number: P=0·0008; orange area:
P=0·0007) and the heritability estimate for orange
was not significantly different from zero, indicating little or no heritability. This suggests that the
sires may have been unable to express their orange
ornamentation because of adverse environmental
conditions. The environment of the Jemez Mountain sires is highly oligotrophic and the fish feed
primarily on algae. I examined the gut contents of
27 guppies in 1987 from the Jemez population and
found all to contain algae, and only one large
female contained a single unidentified insect.
Although nothing is known about the development of orange ornamentation in guppies reared
exclusively on a diet of algae, they are known
to have slower growth rates than guppies fed
Daphnia or Tetramin (Dussault & Kramer 1981).
The controversy between the Fisherian and
adaptive schools of female choice has stimulated
Animal Behaviour, 49, 2
386
much theoretical and empirical research in the
past 10 years. There is now both theoretical
(Andersson 1982, 1986; Hamilton & Zuk 1982;
Pomiankowski 1987a, b, 1988; Grafen 1990) and
empirical (Andersson 1989; Kodric-Brown 1989;
McLennan & McPhail 1989; Hill 1990, 1991;
Ligon et al. 1990; Milinski & Bakker 1990; Møller
1990; Zuk et al. 1990) support for adaptive female
choice, but one major problem still remains. That
problem is demonstrating paternal effects on offspring quality. Paternal effects have been shown
on the growth rates of offspring in toads (Mitchell
1990), junglefowl (Zuk et al. 1990) and guppies
(Reynolds & Gross 1992); however, as yet no
study has demonstrated a positive relationship
between ornament expression and offspring viability or fitness. The breeding experiment reported
here showed that there were maternal effects on
offspring quality, but I was unable to detect
paternal effects.
ACKNOWLEDGMENTS
I thank A. Kodric-Brown, J. Endler, L. Hawkins,
M. Molles and two anonymous referees for
making suggestions on the manuscript. This
research was supported by the Biology Department, Student Research Allocation Committee
and the Biology Graduate Research Allocation
Committee of the University of New Mexico.
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