Download Male mating success and survival in the field with respect to size

Journal of Insect Behavior, Vol. 8, No. 1, 1995
Male Mating Success and Survival in the Field with
Respect to Size and Courtship Song Characters in
Drosophila littoralis and D. montana (Diptera:
Drosophilidae)
Jouni Aspi 1'2 a n d A n n e l i H o i k k a l a t
Accepted May 26, 1994; revisedJune 30, 1994
We investigated the importance of male song and morphological characters to
the male mating success in a two-year field study in natural populations of
D. littoralis and D. montana, We compared the properties of mating flies with
those of a random male sample taken at the same time and place. In D. littoralis
the male's size had no effect on his mating success, while in D. montana small
males had a mating advantage in the field during the first study year. Females
preferred males with short sound pulses in both species. We also examined the
relationship between male morphological and song characters and viability by
collecting male flies in late summer and comparing the means of male characters
to those of overwintered flies the next spring. In D. littoralis male size had no
effect on overwinter survival. In D. montana large flies survived better than
small flies. In both species the shifts in song characters during the winter dormancy were opposite to those caused by sexual selection. Our results, accordingly, imply a possible balance between the forces of sexual and natural selection,
which act in opposing directions on attractive male traits.
KEY WORDS: love songs; morphology; mating success; sexual selection; naturalselection.
INTRODUCTION
Males of most Drosophila species produce songs during courtship by means of
wing vibrations (Bennet-Clark and Ewing, 1968). Several laboratory experi-
Department of Genetics, University of Oulu, FIN-90570, Oulu 57, Finland.
2To whom correspondenceshould be addressed,
67
0892-7553/95/0100-0067507.50/0 © 1995 Plenum PublishingCorporation
b8
Aspi and Hoikkala
ments have suggested that male song has a substantial effect on female mate
choice. These experiments have shown that wingless mutants or wing-amputated
males have reduced mating success (Bennet-Clark and Ewing, 1969; von
Schilcher, t976; Kyriacou and Hall, 1982; Hoikkala, 1988; Liimatainen et al.,
1992) and that the success of wingless males can be restored by subjecting
females to playback songs (von Schilcher, 1976; Kyriacou and Hall, 1982).
Among the boreal D. virilis group species, the male song seems to be an especially important courtship stimulus for the female. Absence of song totally blocks
courtship of some species of this species group (Hoikkala, 1988; Liimatainen
et al., 1992). The structure of male songs in the D. virilis group has been
described (Hoikkala et al., 1982), but it is not known whether intraspecific
variation in song characters has any effect on female mate choice in these species.
Body size may also be an important determinant of male mating success.
The influence of male body size for mating success has been shown in several
species in the genus Drosophila. Generally, large males tend to have an advantage in obtaining copulations (Partridge et al., 1987a; Wilkinson, 1987; Hoffmann, 1987; Taylor and Keki6, 1988; Santos et al., 1988; James and Jaenike,
1992), although not always (Boake, 1989). In insects there may be interaction
between male size, songs and mating success because the songs of large males
differ from those of small males in various ways (see Searcy and Andersson,
1986; Partridge et al., 1987b, Tuckerman et al., 1993).
Two sexual selection models have different predictions about the observable
changes in attractive male traits due to sexual and natural selection. In the
"Fisherian" or "arbitrary trait" models of sexual selection (Fisher, 1958; Lande,
1981; Kirkpatrick, 1982; Pomiankowski et al., 1991), the sexually selected male
character is costly, and the models predict that in populations assumed to be in
evolutionary equilibrium, the forces of sexual and natural selection should act
in opposing directions on attractive male traits (Lande, 1981; Bradbury and
Anderson, 1987; Arnold, 1983; Heisler and Curtsinger, 1990). In the "viability
indicator" models (Zahavi, 1975, 1977) the male character is also initially
costly, but the cost of the male character cannot necessarily be observed in the
field. In the original (Zahavi, 1975), "pure epistasis" model (see Iwasa et al.,
1991) natural selection tends to weed out males with low viability and full
expression of the male character. In another major variant, the "conditional"
viability indicator model (Zahavi, 1977; Andersson, 1986; Pomiankowski, 1987;
Tomlinson, 1988; Iwasa et al., 1991), the sexually selected trait is plastic and
reflects male phenotypic quality. Males in good condition may both express the
sexually selected character more fully and show higher survival than inferior
phenotypes. According to these models there may be thus even a positive correlation between the male character value and survival in field tests (e.g., Zeh
and Zeh, 1988).
Determinants of Male Mating Success in Drosophila
69
In this paper we have studied the association of morphological characters
and male song structure with male mating success in the field among the two
most abundant boreal D. virilis-group species (D. littoralis Meigen and D.
montana Stone, Griffen & Patterson). We also studied the association between
male characters and overwinter survival to examine whether the preferred characters are deleterious and whether there is a balance between natural and sexual
selection in the field.
Boreal species of the D. virilis group offer a number of advantages in
studying sexual selection fulfilling most of the structural assumptions premised
in sexual selection models (see Andersson, I987). The species are polygynous
and have no parental care. They are almost or completely univoltine, the successive generations being reproductively isolated. The main viability selection
occurs before the flies mate, i.e., during the larval stage and winter diapause.
Because the flies overwinter as adults, and the mating season in early spring is
very short (Lumme et al., 1978; Aspi et al., 1993) the varying ages of flies
cannot affect male mating success as in other Drosophila species (see Long et
al., 1980; Santos et al., 1988; Hoffman, 1990).
MATERIALS AND M E T H O D S
Male Mating Success in the Field
We investigated the importance of male morphological and song characters
to mating success by comparing the properties of mating flies with those of a
random sample taken at the same time and place in natural populations of D.
littoralis and D. montana. Collections were made on 7 days between May 5
and June 1 in spring of 1988 and on 6 days between April 28 and May 24 in
spring of 1989 in northern Finland (65°40'N, 23°35'E). These sampling periods
cover the whole mating season of the species (see Aspi et al., 1993). The flies
were trapped by exposing plastic jars baited with fermenting malt to flies for
several hours. Jars were covered frequently by a net and the mating pairs as
well as solitary flies were gently removed with an aspirator. Samples of flies
were caught also on birch (Betula pubescens) sap fluxes in spring of 1988. Since
no differences in the studied characters (see below) between flies collected on
malt baits and on sap fluxes were found, the samples were pooled. The collection
methods are provided in detail by Aspi et al. (1993).
Male Overwinter Survival in the Field
Since the winter diapause is the longest and probably the most demanding
life stage in the adult life, we examined the relationship between male characters
and viability by collecting the newly emerged male flies in late summer 1988
70
Aspi and Hoikkala
and comparing the means of male characters among young flies to those of
overwintered flies belonging to the same cohort in the spring of 1989.
Morphological Measurements
Three linear measurements were made on each male: the length of the
thorax, the length of the wing, and the width of the wing. The left wing and
the body were mounted on a glass microscope slide covered with a thin layer
of glycerol, and the measurements were made using a dissecting microscope
with an ocular micrometer. Wing width was measured from the intersection of
the second longitudinal vein and the distal wing margin to the intersection of
the fifth longitudinal vein with the distal wing margin. Wing length was measured along longitudinal vein 3 from the anterior cross vein to the intersection
with the distal wing margin. For statistical analysis each measurement was
transformed to natural logarithms.
Courtship Songs
The songs of the wild-caught males were recorded in the laboratory, when
the males were courting conspecific laboratory-reared females in a plastic netcovered petridish (diameter, 50 mm; height, 12 mm). Song recordings were
made with a JVC condenser microphone and a Sony TC-FX 33 cassette recorder.
Oscillograms of the songs were analyzed by a Gold 1425 digital oscilloscope.
The song of D. littoralis consists of discrete sound pulses (Fig. 1). For
this species we analyzed five sound pulses per male. We measured the length
of each sound pulse (henceforth PL) and the distance from the beginning of the
pulse to the beginning of the next one (IPI) and counted the number of cycles
in each pulse (CN). The song of D. montana consists of trains of sound pulses
(Fig. 1). For this species we analyzed the fourth sound pulse from five pulse
trains as in D. littoralis and counted the number of pulses (PN) and measured
the length of the pulse train (PTL) in each pulse train. Means were then calculated for each character over these five sound pulses (in D. littoralis) or five
pulse trains (in D. montana) to decrease within-male variation in song characters. For statistical analysis PTL, IPI, and PL were transformed to natural
logarithms in both species. The repeatabilities of all these song characters are
generally rather high (Aspi and Hoikkala, 1993).
Statistical Analysis
The statistical analysis of male characters involved estimation of selection
differentials and selection gradients. Directional selection differentials are the
differences between the mean value of a trait before and after selection and
represent the total effect of selection (Falconer, 1981; Lande and Arnold, 1983;
Determinants of Male Mating Success in Drosophila
71
A
- -
SOUND CYCLE
SOUNO PULSE
INTERPULSE INTERVAL (tPI)
B
-- SOUND CYCLE
SOUND PULSE
INTERPULSE INTERVAL (IPI)
PULSE TRAIN
I
I
100
1
200
1
300 ms
Fig. 1. Oscillogmms of cou~ship songs of wild-caught males in D. littoralis (A)and in D.
montana (B).
Endler, 1986). The directional sexual selection differentials were estimated as
the difference between the mean character value for copulating males and mean
pooled character value for all the males (Lande and Arnold, 1983). To examine
whether the selection differentials in the 2 years were different, we tested whether
the deviations from the mean of the two classes differed between the years. This
procedure is analogous to Levene's test (e.g., Snedecor and Cochran, t980).
The directional natural selection differentials for different characters were estimated as the difference in means of the fall and spring population.
Following Endler (1986) we use term variance selection (stabilizing or
disruptive) for selection affecting the variance of phenotypic traits. Variance
selection differentials were estimated only when the fitness maximum (or minimum) occurred at some intermediate point of the phenotype distribution (see
Mitchell-Olds and Shaw, 1987). Variance selection differentials for these characters were calculated as the difference between the variance for the two groups
of males, subtracting the changes due to directional selection (Lande and Arnold,
1983).
All morphological characters were significantly correlated within both species. The correlations between song characters varied, the highest being between
PL and CN in both species and, also, between PTL and PN in D. montana (see
Hoikkala and Lumme, 1987). All correlations between morphology and song
characters were low ( < 0.3). Because the studied characters within both variable
sets were correlated, the observed changes in phenotypic means could be due
72
Aspi and Hoikkala
to indirect selection affecting a correlated character. Thus we also estimated
selection gradients for each trait to measure the direct effects of selection in
each trait independent of any indirect effects caused by selection on other characters (Lande and Arnold, 1983; Arnold and Wade, 1984a,b).
Because our study approach to both selection episodes was cross-sectional
rather than longitudinal (Arnold and Wade, 1984b), the normally used multiple
partial regression was not appropriate. Instead directional selection gradients
were calculated by multiplying the standardized selection-differential vector by
the inverse of the phenotypic variance-covariance matrix (Lande and Arnold,
1983). Significance levels for selection gradients could not be estimated but
these gradients are still valuable when considering possible contrasts between
selection differentials and gradients.
Sexual selection differentials and gradients were estimated for both years
and also for pooled data if the selection differentials were not different between
years. Because the numbers of males in different variable sets were not equal,
and due to low correlations between character sets, the morphology and songs
were analyzed separately to maximize the sample sizes and to simplify interpretation of results of statistical analysis.
The methods described by Lande and Arnold (1983) can sometimes give
misleading results depending on the form of the fitness function in the range of
the character (MitchelI-Olds and Shaw, 1987; Schtuter 1988). Although only
selection coefficients matter under the model of Lande and Arnold (1983), Turelli and Barton (1990) have shown that the entire shape of the distribution of
the fitness function can influence evolutionary dynamics. These reasons provide
motivation for nonparametric descriptions of fitness surfaces, as proposed by
Schluter (1988). Fitness functions were estimated using the nonparametric cubicspline technique (Schluter 1988), which provides a univariate nonparametric
estimate of fitness probabilities across the range of the considered character.
The estimation of selection gradients involves also other than statistical
assumptions (Lande and Arnold, 1983; Endler 1986; Mitchell-Olds and Shaw,
1987; Rausher, 1992). In our study they may involve unmeasured male characters influencing mating success and environmental correlations between male
characters and success. Inferring causal relationships regarding the effects of
phenotypic characters on fitness on the basis of selection gradients should thus
be made cautiously (e.g., Mitchell-Olds and Shaw, 1987).
Estimation of Variance in Copulatory Success Among Males
Selection coefficients are normally expressed in units of standard deviation
(selection intensity s e n s u Falconer, 1981). Estimation of standardized sexual
selection coefficients requires an estimate of the variance in male mating success
(Amold and Wade, 1984a,b). In insects variance can be estimated in the field
only rarely (e.g., McLain, 1987, 1991; several authors in Clutton-Brock, 1988).
Determinants of Male Mating Success in Drosophila
73
It has been suggested that the proportions of copulating and solitary males can
be used to estimate the variance in male mating success (e.g., Arnold and Wade,
1984b). However, in our case the males were scanned only once. Since even
the most attractive can not be in copula constantly, this approach will give
overly large variance estimates for male mating success. Accordingly, to get a
more reliable estimates we used an approach similar to Zuk (1988; see also
Markow and Sawka, 1992), where variance in male mating success was estimated in separate mate choice experiments.
For the estimates of variance in male mating success random samples of
flies were caught on May 1, 4, and 13 in 1989. Males were identified, but
because it is not possible to identify the species of female flies on the basis of
external traits, the female samples consisted of a mixture of D. virilis group
species. Two experiments were conducted. In the first all females and D. montana males caught on May 1 were used; in the second females and D. littoralis
males caught on May 4 and 13 were used. The sex ratios and alien female
species composition were thus similar to those faced by the males in the field
(see Aspi et al., 1993).
Observations were made using a mating chamber, which was large enough
(16 cm in height, 17.5 cm in breadth, and 24.5 cm in length) for a female to
terminate the courtship. To make the external circumstances as natural as possible the experiments were performed in a climate room, where the temperature
was 12°C. The relative humidity within the chamber was 70%.
Prior to the experiment, the females were aspirated into the chamber and
allowed to habituate for 5 min. After the habituation period, all the males were
aspirated into the chamber simultaneously. The copulating pairs were caught
with an aspirator, examined without anesthesia with a dissecting microscope,
and marked with a small dot of acrylic paint on the ventral surface of the thorax.
If the individual was already marked, we used a different color to make the next
mark. After marking, the flies were released back into the chamber. The treatment lasted no longer than the copulation duration of these flies [4 to 6 min
(Aspi, 1992)]. The experiment was continued until as many copulations were
observed as there were males present. The frequency of mated and nonmated
individuals was used to obtain a weighted variance for calculating standardized
selection differentials and gradients using the formula provided by Zuk (1988).
Standardized variances of copulation success were calculated as the variance of
the matings divided by the square of the mean number of matings (Wade and
Arnold, 1980).
RESULTS
Variance in Male Copulation Success in the Laboratory
In the experiment to estimate the variance in male copulation success the
number of copulations per male ranged from zero to four in both species. The
distribution of copulations among males is listed in Table I, together with the
Aspi and Hoikkala
74
Table I. The Distribution of Numbers of Male Matings Observed and Expected in Mating
Chamber Experiments in Two Drosophila Species"
No. of matings
D. littoralis
Observed
Expected
D. montana
Observed
Expected
0
1
2
3
4
/
N
D
35
22.9
4
21.7
6
10.0
13
3.6
1
0.6
1.75
59
0.361"
35
23.7
6
21.7
3
9.9
13
2.9
2
0.7
1.86
59
0.368*
IIII III
"N is the number of males used in experiment, t is the standardized variance of the copulatory
success, and D is the test value of the Kolmogorov-Smirnovtest.
*Significant with Kolmogorov-Smimovtest at level P < 0.01.
Poisson distribution, which is expected if the mating time is short compared to
total time of the experiment (Sutherland, 1985). The duration of the experiment
was 9 h 20 min in D. littoralis and 10 h 15 min in D. montana. Since the
copulations in both species last only for 4 to 6 min, each courtship occupied
only a negligible fraction o f the total experimental time. The goodness of fit of
observed versus expected Poisson distribution was tested using the KolmogorovSmimov test (Table I) and also a dispersion test suggested by Sutherland (1985).
The distribution of copulations deviated significantly from random in both tests.
The observed frequencies were greater than expected in the tails and less
than expected in the center of the distribution data in both species, i.e., some
males were more successful and some less successful than expected. The estimated standardized variances in copulatory success may be even conservative
as the capturing and painting process probably disturbed the treated males.
Male Morphology and Mating Success in the Field
Male size had no effect on mating success in D. littoralis. The means of
the morphological characters of the males found in copula did not differ from
the mean o f solitary males in either o f the years (Table II). The fitness function
presented for the first principal component (general size; Fig. 2A) explains 85 %
of the total variation in morphological characters. It decreases monotonically
(as well as fitness functions for separate characters), suggesting that variance
selection is not present.
In D. montana the smaller males were more successful in achieving copulation than larger males in 1988 (Table II), but in 1989 there were no significant
differences between the males found in copula and solitary males. The selection
differential estimates for thorax length were significantly different between years,
(N
1.30
2.23
1.30
D. montana
Thorax length
Wing length
Wing width
= 28)
5:0.02
5:0.04
5:0.03
= 38)
5:0.02
+ 0.02
+ 0.01
=
+
+
+
80)
0.01
0.01
0.01
(N = 126)
1.36 5:0.01
2.26 5:0.01
1.33 5:0.01
(N
1.41
2.28
1.36
Solitary
s'
-0.515"
-0.196
-0.239
-0.028
-0.144
0.032
i
-1.096
0.385
0.325
0.175
-0.618
0.406
/3'
(N
1.35
2.27
1.34
(N
1.39
2.24
1.28
= 50)
5:0.02
5:0.02
5:0.01
= 32)
5:0.01
5:0.02
+ 0.02
Copulating
1989
=
+
+
+
97)
0.01
0.01
0.01
(N = 147)
1.33 5:0.01
2.25 5:0.01
1.32 5:0.01
(N
1.39
2.26
1.24
Solitary
i
0.087
0.150
0.180
0.019
-0.078
0.014
s'
-0.192
0.088
0.256
0.094
-0.296
0.185
[3'
"Means (+SE) for males found in copula and solitary males are provided, and in parentheses are the number of males studied. Directional sexual selection
differentials (s') and gradients (,6") are given in units of standard deviation.
* P < 0.05; t test between the means of copulating and solitary males.
(N
1.41
2.25
1.36
Copulating
D. littoralis
Thorax length
Wing length
Wing width
Character
1988
Table il, Male Morphology and Mating Success in D. littoralis and D. montana in 1988 and 1989"
....,I
.....
76
Aspi and Hoikkala
A 1.o 1 ~ 1 9 8 8
B
--1989
1.0
--t988
--1989
I
0.8
f 11
0.6
- ~
0,6-
0.4
0.4~
I
0.2
0.2
u
u
E
0,8
/~'~"
0.0
0,0
--6
-4
--2
0
2
Generol size (PC1)
4
~ / ' ~
-6
,~/
-4
/ ~" ~" ~ ' /
/
-2
0
2
4
t5
Generol size (PC1)
Fig. 2. Nonparametricfitness functions for male mating success in relation to general size in D.
littoralis (A) and in D. montana (B).
and thus the means and selection coefficients are not given for pooled data. In
D. montana the first principal component also explained most (90%) of the
multivariate variation in morphological characters. The fitness function for the
first principal component shows bimodality in male size in relation to fitness in
both years (Fig. 2B). Accordingly, the relationship between male relative fitness
and morphological characters may be more complicated than that of the parametric model of Lande and Arnold (1983). The selection gradients (Table II)
may be misleading and the importance of separate characters to male mating
success cannot be evaluated. Existence of disruptive selection with respect to
male size in D. m o n t a n a in 1988 was supported by the fact that the variances
of all morphological characters were larger among the mated males than among
solitary ones. Variance selection differentials in 1988 for thorax length, wing
length and wing width were 0.95 (F = 2.01, P < 0.05), 0.89 (F = 2.22, P
< 0.01), and 1.16 (F = 2.65, P < 0.001). In 1989 there were no differences
in variances between different groups.
Male Courtship Songs and Mating Success in the Field
The fitness functions of all song characters in D. littoralis were monotonically increasing or decreasing indicating no variance selection. The means of
song characters differed significantly (t test, P < 0.001 for each character)
between the study years, and thus the means for pooled data are not given. In
the second year the males had shorter IPIs and sound pulses (PL) and lower
number of cycles in a pulse (CN) compared with the first year (see Table III).
In D. littoralis there was also some inconsistency in selection differentials
between the years (Table IH), although the differences were not significant. In
1988 there were no significant differences between the means of mating and
(N = 38)
58.1 5 : 1 . 2
356.4 5 : 7 . 6
17.8 5 : 0 . 4
(N = 28)
271.4 ± 6.9
8.6 5 : 0 . 2
14.27 5 : 0 . 4
26.06 5 : 0 . 4
4.7 5:0.1
D. littoralis
PL
IPI
CN
D. montana
PTL
PN
PL
IPI
CN
(N =
279.3
8.7
15.4
26.5
5.0
113)
± 4.2
± 0.1
5:0.3
± 0.2
5:0.1
(N =* 80)
59.0 5 : 0 . 9
345.1 5 : 4 . 5
17.6 ± 0.2
Solitary
-0.131
-0.102
-0.252*
-0.118
-0.161
-0.070
0.t69
0.075
s'
0.050
-0.175
-0.312
-0.099
0.066
-0.250
0.225
0.170
/~'
(N = 47)
248.0 5 : 4 . 8
8.4 5:0.1
14.4 5 : 0 . 4
27.5 5 : 0 . 3
4.4 ± 0.1
(N = 23)
44.1 5 : 1 . 0
262.2 + 9.1
14.8 5 : 0 . 3
Copulating
(N = 83)
243.9 5 : 3 . 5
8.1 __. 0.1
16. t 5 : 0 . 4
27.7 5 : 0 . 5
4.5 _+ 0.1
(N = 73)
48.2 :i: 0.7
283.1 + 5.6
16.1 5 : 0 . 3
Solitary
1989
0.084
0.209*
-0.340**
0.023
-0.043
-0.527**
-0.340
-0.458**
s'
iii
-0.133
0.271
-0.516
0.289
0.274
-0.338
-0.271
-0.192
f3'
0.037
0.091
-0.311"*
-0.031
-0.089
0.249*
-0.025
-0.129
s'
~'
-0.060
0.073
-0.526
0.113
0.287
-0.299
0.050
0.056
1988-1989
"Means (+SE) for males found in copula and solitary males are provided, and in parentheses are the number of males studied. Directional sexual selection
differentials (s') and gradients (/~') are given in units of standard deviation.
* P < 0.05; t test between the means of copulating and solitary males.
* * P < 0.01; t test between the means of copulating and solitary males.
Copulating
Character
1988
Table 111. Male Song Characters and Mating Success in D. littoralis and D. montana in Years 1988 and 1989"
gl
IIQ
ga
m
~a
78
Aspi and Hoikkala
solitary males, but in 1989 copulating males had significantly shorter sound
pulses (PL) and fewer cycles per pulse (CN) than solitary males. The selection
gradients for PL were rather consistent, and also the largest ones in both years
and in pooled data, suggesting that PL was the target of female choice (Table
HI). Obviously females seem to prefer shorter pulses in this species. Selection
gradients for the other characters were not similar in different years, probably
because they are sensitive to small perturbations in data containing closely correlated characters (e.g., Endler, 1986). Accordingly, the interpretation of selection gradients was based on pooled data, since it would give the most reliable
results. These gradients suggest that strong direct female preference for short
pulses produced an indirect selection to decrease CN in 1989, although it was
not itself a target of female choice.
In D. montana there were no significant differences in the means of song
characters between the study years. The length of a pulse (PL) was shorter
among copulating males than among solitary males in both study years, and in
1989 also the number of pulses in a pulse train (PN) was larger among copulating
males than among solitary males (Table HI). In this species, there were no either
significant differences in selection differentials between years. The magnitude
of selection gradients for PL and CN in the pooled data were at least twofold
larger than the values for other characters, suggesting that these characters were
the main targets of female preference. The significant increase in PN in 1989
was probably only an indirect product of direct preference for short PL, which
is negatively correlated with PN. The second largest selection gradient for CN
was positive suggesting direct preference for more sound energy per pulse,
although there was no significant difference in the mean of this character between
the two groups in either years or in pooled data.
Male Morphology and Overwinter Survival in the Field
In both species all the fitness functions for principal components (Fig. 3)
as well as separate characters were monotonically increasing. In D. littoralis
the means of the males of the late summer and the spring populations did not
differ for any morphological characters studied, whereas in D. montana there
were significant differences in the means of all characters (Table IV). Generally,
larger males seem to have survived better during the winter dormancy. According to the selection gradients the main target of selection was the width of the
wing. Since the smaller males were more successful in obtaining copulations
during the mating season and the magnitudes of sexual and natural selection
differentials were quite similar, there seems to be a balance between sexual and
natural selection in D. montana.
Determinants of Male Mating Success in Drosophila
A,0
~1.0
79
[
I
0.8
0.8
0,6
0,6
o
.>
.=
_o
0.4
0.4
J
/
0.2
0.2
0.0
-6
.....i
i
i
i
i
-4
-2
0
2
4
0.0
6
I
-8
-6
-4
-2
O
2
"4
G e n e r o l size ( P C 1 )
Generol size (PC1)
Fig. 3. Nonparametric fitness functions for male overwinter survival in relation to general size in
D. littoralis (A) and in D. montana (B).
Male Courtship Songs and Overwinter Survival in the Field
The fitness functions of the male winter survival for song characters did
not have any modes or dips in either species. In D. littoralis all song characters
were significantly different in autumn and in spring populations (Table V). The
net result of viability selection in PL and CN was opposite to sexual selection,
i.e., the overwintered males had longer sound pulses including more sound
cycles than the males of the late summer population. According to the selection
gradients PL was the probable target of viability selection, and during the winter
dormancy males with long pulses were favored.
In D. montana the selection differentials for most song characters were
opposite in sign to the selection differentials of sexual selection (Table V). Only
the selection differentials for PNs and IPIs were significantly different in the
late summer and spring populations. PN and PL had the largest selection gradients indicating that they were the main targets of selection. The direct selection
was opposite to sexual selection in PN but not in PL. The net changes in these
characters were, however, opposite in sign compared to the changes due to
sexual selection. Thus it seems that also in this species the changes in songs
during the winter dormancy were opposite to those caused by sexual selection,
although the targets of sexual and natural selection may not have been the same.
DISCUSSION
The results of the present study suggest that the magnitude of sexual selection on male characters may vary between years. In D. littoralis the size of the
courting male appeared not to be critical to male mating success, whereas in D.
1.36 5:0.01
2,23 + 0.01
1.31 5:0.01
Thorax length
Wing length
Wing width
1.39 5:0.01
2.25 5:0.01
1,33 5:0.01
Spring
(N = 113)
0.171
0.066
0.159
s'
0.234
-0.365
0.318
/~'
1.30 5:0.01
2.15 + 0.01
1.27 + 0,01
Autumn
(N = 215)
1.33 5:0.01
2.26 5:0.01
1.32 5:0.01
Spring
(N = 183)
D. montana
0.370*
0.358*
0.555*
s'
-0.171
-0,639
1,099
~'
"Means (+SE) for autumn and spring populations are provided. Directional sexual selection differentials (s') and gradients (/~') are given in units of
standard deviation.
* P < 0.001; t test between the means of autumn and spring populations.
Autumn
(N = 296)
Character
D. littoralis
II
Table IV. Male Morphology and Overwinter Survival in D. littoralis and D. montana"
P.
an
t~
llll,i i
iiiiiiiiilllll
.
.
42.4 _ 0.7
293.2 + 5.2
14.16 + 0.3
.
.
47.2 + 0.6
278,1 + 4.9
15.8 5:0.2
.
.
Spring
(N = 96)
0.933***
-0.476*
0.739**
.
.
s'
IIIIIIIIIII I I
IIIIIIIII
1.019
-0.683
-0,053
/3'
IIIII I
247.9
9.7
14.6
24.3
4,4
INIIIIII
+ 8.0
+ 0.4
5:0.7
+ 1.1
+ 0.2
Autumn
(N = 27)
I IIIIIII
--I- 2,8
+ 0, 1
+_ 0.3
_ 0.4
+ 0,1
Spring
(N = t30)
245.4
8.2
15.5
27.6
4.4
III IIIIIIII
D. montana
I
-0.055
-0.836**
0.266
0.621"*
0.066
s'
0,448
-1.597
-0.969
0,303
-0,412
/3'
"Means (+SE) for autumn and spring populations are provided. Directional sexual selection differentials (s') and gradients (/3') are given in units of
standard deviation.
*P < 0.05; t test between the means of autumn and spring populations.
**P < 0.01; t test between the means of autumn and spring populations.
***P < 0.00[; t test between the means of autumn and spring populations.
PTL
PN
PL
IPI
CN
Character
Autumn
(N = 49)
D. littoralis
Table V. Male Song Characters and Overwinter Survival in D, littoralis and D. montana"
Bo
,,,I
ran
I=
m
82
Aspi and Hoikkala
montana small males had a mating advantage, but only during one of the study
years. Both D. littoralis and D. montana females appeared to prefer the males
with short sound pulses. In D. montana the preference was significant during
both study years, but in D. littoralis only during the second year. These results
indicate that the mating success of certain types of males is not so definite as
laboratory experiments often lead us to think. The mating success of different
types of males depends largely on the environmental conditions and on the
phenotypic variation among the available males in field, being not solely due
to sexual selection exercised by the females. Due to the masking effects of these
factors, the real targets of sexual selection may be difficult to find out in the
field.
Male mating success with respect to size has been studied in several natural
populations of Drosophila (Partridge et al., 1987a; Taylor and Keki6, 1988;
Santos et al., 1988; James and Jaenike, 1992), and in all of these studies large
males have appeared to be more successful in obtaining matings than small
males. In D. montana the small males, if any, appeared to have a mating
advantage. Because of the better maneuverability of a small body compared with
a large one, the small males may have a mating advantage in circumstances
where agility is an important component of mating success (McLachlan and
Allen, 1987; Steele and Partridge, 1988). However, the possible reason for the
difference between our results and the previous field studies may lie also in the
possibility that the better mating success of large males in some Drosophila
species is due not to female choice but to direct contests or scramble competition
between males (Partridge et al., 1987b; Wilkinson, 1987) and that the importance of male contests on mating success may vary in different kinds of mating
systems or ecological conditions (see Markow and Ricker, 1992). Direct contests
favoring male-male competition ability and large size will be important determinants of male mating success in circumstances where small ephemeral resource
patches are available (see Hoffmann and Cacoyianni, 1989). Scramble competition is mostly adaptive in crowded conditions which probably prevail in natural
populations of D. melanogaster (Crossley and Wallace, 1987). In D. littoralis
and D. montana direct fights between males are rare (Liimatainen et al., 1992;
Aspi et al., 1993; Hoikkala and Aspi, 1993), and small resource patches seem
to be absent during the mating season of these species (Aspi et al., 1993).
Because the boreal populations of Drosophila are rather sparse, scramble competition between males may not be as important component of male mating
success as among Drosophila in other ecological contexts.
The mating success of small D. montana males was better than that of the
large males during only one of our study years, suggesting that it was affected
by other factors than active female choice. The sizes of the available males may
also depend on environmental factors. Stalker (1980) has suggested a sizedependent relationship between temperature and flying ability of Drosophila.
Determinants of Male Mating Success in Drosophila
83
He found that small flies have relatively large wing-load indices (ratio between
thorax volume and wing area), and they can fly in colder temperatures than
large flies. When calculating the wing load indices of flies in our data, we found
significant differences between collecting days in this ratio in D. montana in
spring 1988 (F = 4.05, P < 0.01, df = 4,147), but not in spring 1989 (F =
1.86, P > 0.1, df = 5,156). In spring 1988 the wing-load index was significantly correlated with mean daily temperature (r = -0.921, P < 0.05). Because
small flies have relatively large wing-load indices also in our data (correlation
coefficient between wind load index and general size, r = - 0 . 2 8 7 , P < 0.001),
they could probably fly in colder temperatures than large flies. The mean daily
temperature of collecting days in 1988 was only 2.7°C, while in spring 1989 it
was 7.7°C. This might explain why the smaller males were selectively favored
in the cold spring of 1988 but not in the warmer spring of 1989. Thus although
there was mate choice with respect to size (as defined by Halliday, 1983), there
was not necessarily female preference or "active" female choice (see Halliday,
1983; Parker, 1983).
In some other animal groups structural song characters can give cues about
male size (Tuckerman et al., 1993). However, we found only low correlations
between morphological and song characters. This is consistent with other Drosophila studies, in which no significant correlations between structural song
characters and size have been found (Partridge et al., 1987).
Several laboratory experiments have shown that the presence or absence of
song affects female choice in Drosophila (Bennet-Clark and Ewing, 1969; yon
Schilcher, 1976; Kyriacou and Hall, 1982; Hoikkala, 1988; Liimatainen et al.,
1992). The only attempts, so far, to study the importance of variation within
the species in song characters on female choice has been carried out by Cowling
(1980) and Greenacre et al. (1993). In Cowling's study the range of IPIs in
male songs was equally acceptable to the females in D. melanogaster. Cowling
(1980) also tried to examine the past selective events which might have affected
the songs in their history using a diatlel analysis. He found that IPI and sine
song frequency were characterized by a high degree of additivity and no significant dominance, indicating that no directional or stabilizing selection had
altered these characters during their past history. Greenacre et al. (1993) have
studied preferences of females homozygous for mutant p e r allele, which alter
rhythmic components of male song. In this study the females carrying the p e r
mutant also preferred wild-type over mutant songs.
In our study both D. littoralis and D. montana females appeared to exercise
selection on male courtship songs preferring males with short sound pulses and
in D. montana probably also males with lot of sound energy per pulse. Because
the songs are not used in male contests, we believe that the association between
male song characters and mating success is due to female preference (cf. Searcy
and Andersson, 1986). The selection for short PL in D. littoralis was evident
84
Aspi and Hoikkala
only in spring 1989. This could be because all males had longer sound pulses
on average in 1988 than in 1989, and the females may not have had favorable
males to choose from. We have previously shown (Hoikkala and Aspi, 1993)
that the number of courting males may affect female choice with respect to male
song. A female can accept a male producing less favorable songs, if there are
no other males available. As mentioned above the spring of 1988 was cold and
the number of males courting the female may have been lower than in the warmer
spring of 1989, and thus the differences in selection differentials may reflect
relative mate choice.
The only attempt so far to examine the balance between sexual and viability
selection in Drosophila has been made by Wilkinson (1987). He estimated the
intensity of sexual and viability selection on male wing length under laboratory
conditions in a recently captured D. melanogaster population. After estimating
the heritability of the character, he found that the expected standardized response
due to sexual selection was opposite in sign and similar in magnitude compared
to the standardized response due to viability selection. The results of the present
study suggest a balance between sexual and natural selection in some male
characters in both species. The large males survived better during the winter,
but the small males may have had an advantage in obtaining copulations in D.
montana. The changes in the song characters during the winter were opposite
to those caused by sexual selection in both species. In D. littoralis the targets
of both sexual and natural selection in song characters were the same. In D.
montana the shifts in song characters during the winter dormancy were also
opposite to those caused by sexual selection, even though the targets of sexual
and natural selection were different. However, as Heisler (1985) has shown, the
balance between natural and sexual selection can be obtained even if the targets
of different selection episodes would not be the same. The results of the present
study thus fulfil the predictions of the "arbitrary trait" model of the balance
between two selection episodes, given that the observed changes in male songs
during diapause are due to selection.
We cannot, however, reject the possibility that the difference between the
means of the males of the summer and spring populations were due to other
factors than selection. Our attempts to maintain these flies overwintering in
outdoor chambers in winters 1988-1989 and 1989-1990 to estimate survival
rates and assign individual fitness values to overwintering flies were not successful. Changes in means of song characters may thus be due to changes in
the songs of individual males during the winter dormancy, males may have
migrated selectively from the area, or our traps may not have been equally
attractive to different phenotypes in different seasons. Assuming that the changes
in the means of song characters are due to changes within individual males, this
observation could also be accommodated by the viability indicator model. I f the
altered songs reflect the phenotypic condition of the males and the songs of
Determinants of Male Mating Success in Drosophila
85
inferior males have c h a n g e d m o s t during the diapause, the females c o u l d h a v e
chosen the " b e s t " males by c h o o s i n g males producing songs, which resemble
those o f freshly e m e r g e d males. If so, this finding could be also c o m p a t i b l e with
conditional viability indicator models.
ACKNOWLEDGMENTS
W e express o u r thanks to P. H e d r i c k , J. L u m m e , T. Shelly, and an anony m o u s referee for their v a l u a b l e c o m m e n t s on the manuscript. D. Schluter kindly
p r o v i d e d us the p r o g r a m to estimate fitness functions.
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