Behavioral Ecology Vol. 10 No. 4: 358-365
© 1999 International Society for Behavioral Ecology
Postmating sexual selection: the effects of male body size and recovery period on paternity and egg production rate in a water strider
a
Department of Animal Ecology, University of
Ume
, SE-901 87
Ume, Sweden
b
Animal Ecology, Department of Zoology, Göteborg
University, Box 463, SE-405 30 Göteborg,
Sweden
Address correspondence to G. Arnqvist. E-mail: Goran.Arnqvist{at}animecol.umu.se
Received 29 April 1998; revised 26 October 1998; accepted 21 November 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The role of male body size in postmating sexual selection was explored in a semiaquatic insect, the water strider Gerris lateralis. To separate effects of male size per se from those due to numeric sperm competition, male recovery period (shown here to be proportional to ejaculate size) was manipulated independently of body size in a factorial experiment where virgin females were mated first with sterile males and then with focal males. Both relative male fertilization success and female reproductive rate were measured. The number of sperm transferred increased with male recovery period, an effect that was mediated by longer copulation duration, but there were no effects of body size on ejaculate size. Neither male size nor recovery period had any significant direct effects on male fertilization success. However, copulation duration influenced relative fertilization success, suggesting that males able to transfer more sperm also achieved higher fertilization success. Females exercised cryptic female choice by modulating their reproductive rate in a manner favoring large males and males that were successful in terms of achieving high relative fertilization success. Thus, successful males gained a twofold advantage in postmating sexual selection. This study has important implications for previous estimates of sexual selection in this group of insects because pre- and postmating sexual selection will be antagonistic due to limitations in male sperm production: males mating frequently (high mating success) will on average transfer fewer sperm in each mating and will hence tend to fertilize fewer eggs per mating (low fertilization success).
Key words: body size, copulation duration, cryptic female choice, ejaculate size, Gerris lateralis, recovery period, reproductive effort, sexual selection, sperm competition, sperm precedence, water striders.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Our understanding of sexual selection and the evolution of mating systems is currently being significantly revised. Empirical and theoretical studies have by tradition dealt almost exclusively with variance in mating success among males as the generator of differential reproductive success and hence sexual selection (see Anderson, 1994
), but many authors now stress the potential importance of
variance in postmating paternity success among males for the evolution of
sexual characters (Arnqvist,
1998; Briskie et al.,
1997; Eberhard,
1985; Harcourt et al.,
1981) as well as mating systems
(Birkhead and Møller,
1992, 1993;
Choe and Crespi, 1997;
Eberhard, 1996). Although the
principal importance of postmating sexual selection has been recognized since
the 1970s (Lloyd, 1979;
Parker, 1970;
Smith, 1984;
Thornhill, 1983), current
knowledge of the causes and effects of variation in paternity success among
males is very limited (Birkhead and
Møller, 1992; Conner,
1995; Eberhard,
1996; Hosken and Stockley,
1998; Lewis and Austad,
1990; Simmons and Parker,
1992).
Nonrandom fertilization success among males can occur as a result of either
competition between male gametes over fertilization (i.e., sperm competition;
Parker, 1970;
Smith, 1984), or as a result
of any of a number of female processes that affect relative male paternity
success (i.e., cryptic female choice;
Eberhard, 1996;
Lloyd, 1979;
Thornhill, 1983). It has
proven difficult to distinguish empirically between these two mechanisms,
especially as they are not mutually exclusive
(Bissoondath and Wiklund,
1997; Simmons and Parker,
1992; Simmons et al.,
1996; Wilson et al.
1997; Wirtz,
1997). Models of sperm competition are typically based on some
form of numerical competition, where the relative success of a male is a
function of the number of sperm transferred by that male
(Parker, 1990;
Parker and Simmons, 1991,
1994;
Parker et al., 1990). There
are at least two different ways in which females can exercise cryptic female
choice (Birkhead and Møller,
1993; Eberhard,
1996). Females can bias paternity by either (1) differential
relative uptake or use of sperm from different males
(Bishop, 1996;
Bishop et al., 1996;
Eberhard, 1996) or (2)
increasing their reproductive effort after mating with a preferred male
(Thornhill, 1983;
Wedell, 1996).
A crucial question in sexual selection theory concerns the kinds of male
traits that are favored by postmating sexual selection, and in particular
whether postmating sexual selection merely reinforces the actions of
conventional premating sexual selection
(Warner et al., 1995). Certain
male traits favored under postmating sexual selection are clearly not under
direct premating sexual selection, such as the shape of male intromittent
genitalia (Arnqvist, 1998;
Eberhard, 1985,
1993) or the chemical
composition of male secondary substances in the ejaculate
(Chapman et al., 1995;
Eberhard, 1996;
Eberhard and Cordero, 1995;
Rice, 1996;
Wilson et al., 1997). Other
traits, however, seem to be important in both pre- and postmating sexual
selection. This is particularly true for overall size. Male body size is not
only the trait most generally favored under premating sexual selection (see
Andersson, 1994), it also seems
to be generally related to relative paternity success (e.g.,
Bissoondath and Wiklund, 1997;
LaMunyon and Eisner, 1993,
1994;
Lewis and Austad, 1990,
1994;
McLain, 1980;
Otronen, 1994,
1998;
Sakaluk and Eggert, 1996;
Simmons and Parker, 1992;
Simmons et al., 1996;
Ward, 1993;
Watson, 1991a,
b;
Wedell, 1991). There are
several reasons that females may benefit from biasing relative paternity in
favor of large males because phenotypic and genotypic quality often are
positively correlated with body size (see
Cordero, 1995;
Johnstone, 1995), but there is
as yet no evidence of adaptive sperm selection by females
(Hosken and Stockley, 1998;
Wirtz, 1997). The fact that
overall body size, or a trait correlated with body size, is positively related
to postinsemination paternity success cannot be taken as evidence for cryptic
female choice (cf. LaMunyon and Eisner,
1993; Ward, 1993)
because body size can be expected to be positively related to the quantity or
quality of transferred sperm and/or accessory substances
(Berrigan and Locke, 1991;
Parker and Simmons, 1994;
Simmons and Parker, 1992). The
effects of body size on paternity can thus result from sperm competition
(Bissoondath and Wiklund,
1997; Simmons et al.,
1996). To disentangle the effects of body size per se from the
quantitative effects of sperm numbers, we need studies that independently vary
male body size and number of sperm transferred (cf.
LaMunyon and Eisner,
1994).
This study represents an attempt to estimate the independent effects of
male body size and number of sperm transferred on paternity success in the
water strider Gerris lateralis (Heteroptera, Gerridae). We achieved
this by measuring the effects of male body size and male recovery period on
both relative male fertilization success and female reproductive effort
subsequent to focal matings, in a factorial experiment with orthogonally
crossed factors. Because male recovery period (i.e., time since last
copulation) is found to have a strong impact on the number of sperm
transferred at each mating, this design allows us to estimate the independent
effects of male size and sperm numbers, thus extending previous attempts to do
so (cf. Bissoondath and Wiklund,
1997; LaMunyon and Eisner,
1994; Simmons et al.,
1996).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Study organism
Water striders inhabit water surfaces of various aquatic habitats both as juveniles and adults and are predators/scavengers feeding mainly on arthropods trapped at the water surface (Andersen, 1982
; Spence and Andersen,
1994). Female water striders of the genus Gerris are
highly polyandrous and may mate several times per day. The mating system is
characterized by male harassment of females and has been described as
convenience polyandry (see Arnqvist,
1997; Rowe et al.,
1994, for reviews). In general, there seems to be weak last-male
sperm precedence, but large intraspecific variation in paternity success has
been documented (Arnqvist,
1988; Arnqvist and Danielsson,
1999; Danielsson,
1999; Rubenstein,
1989). Male G. lateralis may mate several times in rapid
succession (Arnqvist, 1997),
and the relatively small ejaculate consists of little else but sperm
(Andersen, 1982). Average
copulation duration in G. lateralis is 19.5 min (SE = 1.47)
(Rowe and Arnqvist, 1996).
Collection and rearing
During May and June 1997, we collected male and female Gerris
lateralis from populations in Ostnäs and
the River Tavlen, both situated in the
vicinity of Ume, Sweden. The experiments were
conducted in the laboratory, at 20°C (± 2°), under a simulated
natural light regime. Before experiments, females were kept separated from
males in large aerated tanks (1 m diam, water depth 12-20 cm). Males were kept
with nonexperimental females at a sex ratio of approximately 2:1 in aerated
aquaria (25 x 40 cm, water depth 10-15 cm). Both sexes were fed frozen
early instar Gryllus crickets ad libitum and were provided with
styrofoam pieces as resting sites. The water was changed each week and
remaining excess food was removed regularly.
Sterile male technique
We estimated male fertilization success using the sterile male technique
originally described by Parker
(1970). Males were sterilized
by exposure to high-energy X-rays. Males assigned to the irradiation treatment
were collected while mating and isolated from females about 1 h before the
irradiation treatment, which took place between 1600 h and 1700 h the day
before the experimental matings. Males were placed in a petri dish in front of
a linear electron accelerator with 6 MV photon beams. A 14-mm thick disc of
Plexiglas was placed on top of the dish to prevent the water striders from
occupying the dos-buildup area. A water equivalent phantom was placed
underneath for backscattering. Males received an absorbed dose of
130±3% Gy with a dose rate of approximately 10 Gy/min. After
irradiation, males were kept isolated individually in cups (6 cm diam) with
water, food, and Styrofoam pieces. Sperm of irradiated males are able to
fertilize eggs but carry lethal mutations that prevent normal embryonic
development. The irradiation treatment used here is known to decrease the egg
viability rate in this species from the normal 92.2% to 24.9% (see
Arnqvist and Danielsson, 1999).
In the experiments described below, each virgin female was mated with three
males; first with two irradiated males (R1 and R2) and then with a focal
normal male (N). The proportion of viable eggs laid by a female subsequent to
these matings will hence be proportional to the relative fertilization success
of the normal male (P3). This proportion will represent a slight
overestimate of the true value of last-male fertilization success for each
female, but because we dealt exclusively with variance in relative
fertilization success across normal males, we used this proportion as our
measure of fertilization success (see below).
Male size and recovery period
Before the experiment, we used a caliper (0.02-mm resolution) to make
preliminary measures of the body length of all males captured in
Tavlen. Two groups, representing the
approximate 25% tails of the size distribution, were selected as experimental
males (small and large). Postexperimental measures of all individuals, using a
digitizing tablet (Summasketch III) under a side-mounted camera lucida
attached to a dissecting microscope (Leica MZ8), verified that this
preliminary selection had the desired effect: the average body lengths of
small and large males were 7.67 (SE = 0.03) and 8.33 (SE = 0.03) mm,
respectively (t = 10.98, df = 62, p <.001; average body
size difference 9%). The intermediately sized males from the size selection
procedure (mean body length 7.97 mm, SE = 0.02 mm) were assigned to the
irradiation treatment and used as second mates (R2). Irradiated males mating
as first mates (R1) were collected from Ostnäs
and were also of intermediate size (mean body length 8.07 mm, SE = 0.03 mm).
We collected normal males (small and large) from stock aquaria while they were
copulating and thereafter isolated them for either 48 h or 2 h before
experimental matings. These focal males thus form one group with a long and
one with a short recovery period (i.e., time since last copulation). During
this premating isolation, males were kept individually in cups (6 cm diam)
provided with water, food, and Styrofoam pieces.
Experimental matings
To ensure that only virgin females were used, we checked the fertilization
status of individually isolated females before the experiment during a minimum
of 4 days. Females laying any fertile eggs during this period were discarded.
Each virgin female was mated with two irradiated males (R1 and R2), with an
intermating interval of 4-6 h, and with a third normal male (N) on the
following day. The focal N males were either small or large, and had either
long or short recovery period (see above). Thus, the mating design is a
2x2 factorial design (Ntot = 64). In all matings,
copulation time was measured by spot checks each minute, and copulations that
exceeded a maximum duration (2.5 h for R males and 3 h for N males) were
carefully interrupted by gently separating the sexes. Copulation time was
defined as the duration of the period of genital intromission and hence did
not include the postcopulatory noncontact guarding phase
(Arnqvist, 1997). Matings were
staged in plastic jars (15x20 cm, water depth 6 cm).
After the three matings, females were isolated in the mating jars and provided with one thin piece of Styrofoam (2x1 cm) and one piece of balsa wood (2x1 cm) as oviposition substrates. One frozen cricket (length 0.5-1 cm) and one frozen Drosophila fruit fly were added each day. After 4 days, the water was changed and new oviposition substrates were introduced. We collected eggs a second time after another 4 days. The eggs were allowed 8 days of maturation in plastic cups filled with water (20°C), before the number of viable and non-viable eggs were counted (egg age span 8-12 days). Only eggs that showed normal development with red eyespots and legs clearly visible were regarded as viable. Partly developed and opaque eggs were considered nonviable. After 8 days of egg laying, all females were frozen individually in 0.5-ml Eppendorf vials for postexperimental measures of body length.
Control matings
The relationship among ejaculate size, male body size, and recovery period
was established by sperm counts derived from a series of control matings.
Nonvirgin females were isolated for 2 days before control matings. Each female
(Ntot = 36) was then allowed to mate with a normal male
(male treatments as above) in plastic cups (6 cm diam; no water). Copulation
duration was recorded by continuous observation. To prevent sperm
transport/migration from the bursa copulatrix to the spermatheca, females were
frozen individually in Eppendorf vials immediately after the copulation was
terminated. Sperm transport/migration is a relatively rapid process in
Gerris (a matter of a few hours;
Andersen, 1982), so any sperm
in the bursa can safely be assumed to originate from the last mating.
The female gynatrial complex was subsequently removed using a dissecting microscope and placed in 0.5 ml distilled water. The spermatheca was thereafter removed, and the remaining bursa copulatrix (the gynatrial sac) was ruptured. The water and the bursa were transferred to an Eppendorf vial filled with distilled water to a total volume of 1.5 ml and vortexed for 1 min. We placed five subsamples (each of 50 µl) on a microscope slide and allowed them to dry. We then counted the number of sperm within each subsample directly using a microscope (100x).
We estimated ejaculate volume by first measuring the area of each visible
sperm aggregation in the bursa prior to vortexing, by placing a digitizing
tablet (Summasketch III) under a side-mounted camera lucida attached to a
dissecting microscope (Leica MZ8) (see
Arnqvist and Danielsson, 1999).
Ejaculate volume was thereafter estimated based on the assumption that the
shape of each sperm aggregation could be described by an ellipsoid.
Data analysis
The response variable in studies of relative fertilization success is
typically a proportion, but conventional general linear models are
nevertheless applied by tradition. Estimates from such analyses may be biased
not only as a result of the bounded distribution of the response variable, but
more importantly as a consequence of the non-normal and nonconstant binomial
variance and the lack of recognition of the sample size on which each
proportion is based (Aitkin et al.,
1989; Crawley,
1993; McCullagh and Nelder,
1989). To avoid these problems, we chose to estimate the effects
of male size, recovery period, and copulation duration on the proportion of
eggs fathered by the last male to mate (P3) by more appropriate
statistical models. We used a generalized linear model of the number of viable
eggs per female, using binomial errors with the total number of eggs laid per
female as the binomial denominator and a logit link function
(Crawley, 1993). To compensate
for overdispersion (McCullagh and Nelder,
1989), we implemented the method of Williams
(1982) before statistical
inference. Generalized linear models were estimated with GLIM, and all other
statistical evaluations were performed with SYSTAT.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Control matings
The repeatability of sperm counts across subsamples was high (0.922;(F35,144 = 59.33, p <.001) (Lessels and Boag, 1987
),
confirming that our measure of sperm number reliably estimates the number of
sperm contained in a given female's bursa copulatrix. For the analyses below,
we thus used the average sperm count in each mating as the dependent variable.
A two-way analysis of variance of the number of sperm transferred (log
transformed) showed that, as expected, males with a long recovery period
transferred almost twice as many sperm in a given mating as did males with a
short recovery period (average number±SE of sperm in female bursa,
479.3±81.0 versus 245.7±81.0;
Table 1). However, neither body
size nor the interaction between body size and recovery period had any
detectable impact on number of sperm transferred
(Table 1). There were, in
contrast, no effects of male size (F1,32 = 1.56,
p =.221), recovery period (F1,32 = 2.28,
p =.141) or their interaction (F1,32 = 1.99,
P =.168) on sperm transfer rate (log number of sperm transferred /
copulation duration). Hence, we found no support for a higher sperm transfer
rate among large males (cf. Berrigan and
Locke, 1991; Parker and
Simmons, 1994; Simmons and
Parker, 1992) or males with a longer recovery period.
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A two-way analysis of variance of copulation duration (log transformed) showed that males with a long recovery period also copulated for twice as long as did males with a short recovery period (28.0±1.2 versus 13.8±1.2 min; F1,32 = 8.98, p =.005), whereas neither body size nor the interaction between the two had any detectable impact on copulation duration (F1,32 = 0.05, p =.816 and F1,32 = 0.00, p =.999, respectively).
In summary, male recovery period had a strong effect on the number of sperm transferred in a given mating, and this effect was a result of differences between males in copulation durations rather than in sperm transfer rates (see also Figure 1). This interpretation was confirmed by introducing copulation duration as a covariate to the analysis of variance presented in Table 1. In this analysis of covariance, copulation duration (F1,31 = 12.44, p <.001) was the only factor significantly affecting the number of sperm transferred (F1,31 < 1.96, p >.172 for all other factors). Analyses identical to the ones of sperm number, but instead performed on ejaculate volume, gave results that were qualitatively identical and quantitatively similar to those presented above.
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Experimental matings
Sperm precedence
The estimates of sperm precedence of the last male to mate did not differ
during days 1-4 and 5-8 (paired t test on arcsine-transformed data,
t = 439, df = 57, p =.662), and the repeatability over the
two periods in estimated P3 was high (arcsine-transformed data,
r =.765, p <.001). Hence, data from days 1-4 and 5-8 were
pooled for each female to provide an overall estimate of P3. This
forms our measure of the relative fertilization success of the last male in
all subsequent analyses.
Our factorial variables alone (i.e. male size, male recovery period, and
their interaction) did not collectively affect sperm precedence of the last
male (
2 = 3.562, df = 3, p =.313). The copulation
duration of males, however, had a highly significant impact on P3
(log-likelihood ratio test of hierarchical addition of the four mating
duration variables, 2 = 15.461, df = 4, p =.004),
primarily due to effects of the copulation duration of the last male
(Table 2). The fertilization
success of the last male increased with his copulation duration up to
durations of about 60 min, but decreased again in greatly extended copulations
(Figure 2a). In contrast, the
fertilization success of the last male to mate tended to decrease with
increasing copulation duration of the female's previous mates (R1 and R2;
Figure 2b), though this trend
was not significant (Table
2).
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Overall, the intraspecific variance in last-male sperm precedence was strikingly high. The coefficient of variation of arcsine-transformed P3 values was 38.2%. Though highly significant, our model only explained a relatively small proportion of this variation. The deviance ratio of the model presented in Table 2 [(Dnull — Dfull)/Dnull] was 0.367, and the multiple R2 of the corresponding general linear model on arcsine transformed P3 values was.350, both indicating that our model accounted for approximately 35% of the variance in last male fertilization success.
The proportion of the observed variance in copulation duration that was due
to differences among females (cf.
Rubenstein, 1989), as opposed
to among males within females, was small but significant (repeatability across
females of log-transformed copulation duration = 17.7%,
F71,144 = 1.630, p =.007)
(Lessels and Boag, 1987). This
result is in accordance with earlier findings showing that copulation duration
is determined primarily by males in water striders
(Arnqvist and Danielsson, 1999;
Rowe and Arnqvist, 1997).
Female egg production rate
Female egg production rate was not affected by the last male's size or
recovery period (two-way ANOVA; F1,60 < 1.31,
p >.25 in both cases). However, the interaction between these two
factors had a highly significant impact on egg production rate (two-way ANOVA;
F1,60 = 9.728, p =.003). Female egg production
rate increased with male recovery period in large males but decreased with
male recovery period in small males (Figure
3). A series of sequentially Bonferroni adjusted posthoc tests
(Holm, 1979) revealed that
this interaction was primarily due to females mated with small males with a
long recovery period exhibiting a relatively low egg production rate. These
females differed both from those mated with large males with a long recovery
period (t = 3.15, df = 20, p =.004) and those mated with
small males with a short recovery period (t = 3.00, df = 32,
p =.005).
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To further partition variance in female egg production rate, we also performed an analysis of covariance including four covariates: female body size, copulation duration of last male, average copulation duration of previous mates, and the observed degree of sperm precedence. This analysis generated two insights (see Table 3). First, the interaction effect mentioned above was resistant to the inclusion of the covariates and remained an important determinant of egg production rate. Second, when controlling for copulation duration as well a series of other factors, female egg production rate was positively related to the relative paternity success of the last male to mate (Table 3, Figure 4). In other words, females that mated with males that achieved a relatively high fertilization success produced many eggs during the period after that mating.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Our experiments revealed extensive variation in male postmating reproductive success in Gerris lateralis. This was due both to differential fertilization success among males and differences in female offspring production rate after the focal matings. Because the patterns detected in our study differ considerably between these two mechanisms of postmating sexual selection, we discuss these topics separately.
Sperm precedence
We failed to find any direct or indirect effects of male size on relative
fertilization success. Thus, our results do not lend any support to the
general suggestion that females preferentially select sperm from large males
to fertilize their eggs (Eberhard,
1996; LaMunyon and Eisner,
1993; Simmons et al.,
1996; Ward, 1993).
On the contrary, the results strongly indicate that numerically based sperm
competition is a key factor in determining relative male fertilization success
(cf. Parker, 1990). The fact
that copulation duration was the only significant determinant of sperm
precedence supports this interpretation because the number of sperm
transferred in a given mating was directly related to copulation duration. The
fact that sperm precedence was positively related to last-male copulation
duration in copulations of normal length (see Methods), and at least tended to
be negatively related to the copulation duration of previous mates, further
supports this scenario. These results are also in accord with those of
Rubenstein (1989), who found
sperm precedence to be related to the relative copulation duration of the two
males in the water strider Aquarius remigis.
It is unclear why greatly extended copulations were associated with a lower
relative fertilization success, despite the fact that one cwould expect more
sperm to have been transferred in these matings. One possibility is that males
tend to extend the duration of matings with low sperm transfer rates, due to
incorrect genital alignment, for example. Another possibility is that these
males were, with limited success, attempting to avoid complete or partial
female sperm dumping by prolonging copulations. Though female sperm dumping
(i.e., cases where the female discards sperm/ejaculate from the last mating;
Eberhard, 1996), has not been
studied directly in water striders, behavioral observations (Arnqvist and
Danielsson, unpublished) as well as bimodal distributions of sperm precedence
(Arnqvist and Danielsson, 1999;
Danielsson, 1999) suggest that
female sperm dumping may be an important source of variance in male
postinsemination success.
Several authors have pointed out that our understanding of the sources of
variance in sperm precedence is very limited (e.g.,
Eberhard, 1996;
Lewis and Austad, 1990). A
particularly interesting aspect of our results is the relatively low degree of
variance in sperm precedence that was collectively accounted for by our
experimental variables. Though rarely reported, this seems to be the case in
most other studies as well (e.g., Cook et
al., 1997; Lewis and Austad,
1990; Otronen,
1997, 1998;
Rubenstein, 1989;
Simmons et al., 1996). In our
case, this is clearly not due to low statistical power because we maximized
variance in our factorial variables (used only the largest and smallest males
that had experienced either a very short or very long recovery period),
controlled for the important impact of copulation duration, and used a large
number of replicates. Despite this fact, our statistical models accounted for
a minor proportion of the variance in sperm precedence among male G.
lateralis (35%). A larger part of the variance was apparently due to
factors unrelated to male size, recovery period, or copulation duration.
Although variance in estimated sperm precedence will certainly be introduced
by variance in fertility among irradiated males, the fact that the degree of
sperm precedence is repeatable across males in this species
(Arnqvist and Danielsson,
1999), as well as in other insects
(Lewis and Austad, 1990;
Otronen, 1997;
Wilson et al., 1997) strongly
suggests that random factors alone are not responsible for this residual
variation.
A number of phenotypic and/or genotypic characteristics could be important
in determining relative fertilization success. For example, Arnqvist and
Danielsson (1999) demonstrated
that the degree of sperm precedence in this species is affected by the shape
of the male's genital sclerites, showing that variation in male genital
morphology can determine relative paternity success
(Arnqvist, 1998;
Eberhard, 1985). Similarly,
biochemical characteristics of the ejaculate or the sperm cells themselves are
known to affect sperm precedence (see
Eberhard, 1996;
Eberhard and Cordero, 1995).
The success of a given male is also likely to depend in part on the female,
generating an interaction between male and female phenotypic and/or genotypic
characteristics. Such complex patterns of partial or complete incompatibility
between the mates (see Zeh and Zeh,
1996, 1997) has
been shown to affect male fertilization success in several species
(Arnqvist and Danielsson, 1999;
Bishop et al., 1996;
Clark and Begun, 1998;
Hughes, 1997;
Olsson et al., 1996;
Wade et al., 1995;
Wilson et al., 1997) and are
consequential in this context because they suggest that statistical models
including only male characteristics may in general be incapable of accounting
for large proportions of variance in relative male fertilization success.
Female reproductive effort
Two results strongly suggest that female water striders bias paternity in
favor of certain males by modulating the rate of offspring production
following copulation with a given male (i.e., cryptic female choice). First,
female egg production rate decreased with recovery period in small males, a
pattern that was reversed in large males. The fact that females reduced their
egg production rate when mated with small males that transferred a large
number of sperm implies that females possess mechanisms by which they are able
to disfavor small males as fathers of their offspring. This pattern can
clearly not be explained by male-male interactions alone. Second, we found a
positive relationship between P3 and female egg production rate, when
controlling for female size, copulation durations, and a series of other
factors, implying that females invested more in offspring production after
copulations with males that were also relatively more successful in terms of
fertilization. The most parsimonious explanation for this pattern is that
males able to transfer competitively superior ejaculates (e.g., large volume,
many sperm, more mobile sperm, large amounts of accessory substances,
biochemical characteristics) were not only relatively successful in terms of
sperm precedence, but were also better able to stimulate female offspring
production (see Eberhard,
1996). Again, this pattern cannot be explained by male-male
interactions alone, but the effects must be mediated by female mechanisms that
directly or indirectly favor certain males over others.
In insects where male ejaculates contain nutrients that are transferred to
the female (i.e., a nuptial gift), such as in certain butterflies and
bushcrickets, sperm precedence is known to covary with female reproductive
rate (Svärd
and McNeil, 1994; Wedell,
1991; Wedell and Arak,
1989). In such cases, however, this may result from a direct
relationship between the number of sperm transferred and the amount of
nutrients transferred in a given mating because the latter are used by females
for egg production. In other species, females apparently increase their
offspring production rate either when mated with males with large sexual
ornaments or when allowed to freely choose their mate (e.g.,
Burley, 1988;
de Lope and Møller,
1993; Eberhard,
1996; Massa et al.,
1996; McLain and Marsh,
1990; Petrie and Williams,
1993; Simmons,
1987; Swaddle,
1996; Thornhill,
1983). However, few studies have reported a positive covariance
between male sperm precedence and female offspring production rate in species
where no significant paternal investment occurs (cf.
Clark et al., 1995;
Clark and Begun, 1998). A
positive relationship between these sources of variance in male paternity
success have important consequences in terms of postmating sexual selection.
Successful males will have a twofold advantage: they will not only achieve a
high relative fertilization success but will also enjoy a high female
offspring production rate. Thus, future studies should seek to identify the
female mechanisms, as well as the causal male traits, that are responsible for
the pattern documented here.
Sperm depletion and effects on previous estimates of sexual
selection
The production of sperm and accessory substances in the ejaculate involve
certain costs to males, and limitations on male sperm production rate are
manifested as a positive relationship between time since last mating (i.e.,
the recovery period) and the number of sperm transferred in a given mating in
many species (see Dewsbury,
1982; Eberhard,
1996; Møller,
1991; for reviews). Our study showed that male water striders are
no exception to this rule. The number of sperm transferred by males increased
with the recovery period, and male recovery rate was apparently independent of
body size.
Our findings have far-reaching implications for our understanding of sexual
selection in these insects. Numerous studies have shown that male mating
success is positively related to male body size in water striders and have
thus argued that sexual selection favors large males in this group of insects
(e.g., Arnqvist, 1992;
Arnqvist et al., 1996;
Fairbairn and Preziosi, 1994;
Preziosi and Fairbairn, 1996;
Sih and Krupa, 1992). In light
of the results of the current study, it is clear that the relationship between
male body size and reproductive success is more complex than previously
thought and that mating frequency data alone are insufficient to model male
net reproductive fitness. Large size in males may be positively related to
mating frequency and female reproductive effort (see above), but these effects
will at least in part be offset by limitations in male sperm production rate.
Thus, although large males may mate more frequently, small males should
copulate for longer, transfer more sperm in each mating, and hence gain higher
fertilization success per mating due to average longer recovery periods (see
Pitnick, 1991;
Ward & Simmons, 1991, for
similar results in other insects). A strong indication that this scenario is
indeed significant was provided by Rowe and Arnqvist
(1996), who found that
although large males of three different Gerris species mated 15% more
frequently, they also copulated for a 16% shorter period than did small males.
Hence, pre- and postmating sexual selection may often act antagonistically on
male body size, at least in this group of insects. The relative importance of
mating success and postmating fertilization success will to some extent depend
on the gravity of sperm limitation (i.e., the average male mating frequency in
a population—density, reproductive activity, sex ratio), as well as a
series of other factors.
|
ACKNOWLEDGEMENTS |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
We thank Anne Töyrä, Tina Nilsson, Thomas M
rtensson, and Michelle
Arnqvist for assistance with the experiments and Nina Wedell for discussions
on female reproductive rate. John R. Spence and two anonymous reviewers
provided constructive comments on an earlier version of this contribution.
This study was made possible by financial support from The Swedish Natural
Science Research Council to G.A. and from
Rdman och Fru Ernst Collianders stiftelse,
Helge Ax:son Johnsons stiftelse, Larsénska
fonden, and the Royal Swedish Academy of Sciences to I. D. |
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
|---|
Aitkin M, Anderson D, Francis B, Hinde J, 1989.Statistical modelling in GLIM . Oxford: Clarendon Press.
Andersen NM, 1982. The semiaquatic bugs (Hemiptera, Gerromorpha): phylogeny, adaptations, biogeography and classification.Entomonograph vol. 3. Klampenborg: Scandinavian Science Press.
Andersson M, 1994. Sexual selection. Princeton, New Jersey: Princeton University Press.
Arnqvist G, 1988. Mate guarding and sperm displacement in the water strider Gerris lateralis Schumm. (Heteroptera: Gerridae). Freshwater Biol 19:269-274.
Arnqvist G, 1992. Spatial variation in selective regimes: sexual selection in the water strider, Gerris odontogaster.Evolution 46:914-929.[Web of Science]
Arnqvist G, 1997. The evolution of water strider mating systems: causes and consequences of sexual conflicts. In: The evolution of mating systems in insects and arachnids (Choe JC, Crespi BJ, eds). Cambridge: Cambridge University Press;146 -163.
Arnqvist G, 1998. Comparative evidence for the evolution of genitalia by sexual selection. Nature 393:784-786.
Arnqvist G, Danielsson I, 1999. Copulatory behavior, genital morphology and male fertilization success in water striders.Evolution 53:147-156.
Arnqvist G, Rowe L, Krupa J, Sih A, 1996. Assortative mating by size: a meta-analysis of mating patterns in water striders.Evol Ecol 10:265-284.
Berrigan D, Locke SH, 1991. Body size and male reproductive performance in the flesh fly, Neobellieria bullata.J Insect Physiol 37:575-581.
Birkhead TR, Møller AP, 1992. Sperm competition in birds. London: Academic Press.
Birkhead TR, Møller AP, 1993. Female control of paternity. Trends Ecol Evol 8:100-104.
Bishop JD, 1996. Female control of paternity in the
internally fertilizing compound ascidian Diplosoma listerianum. I.
Autoradiographic investigation of sperm movements in the female reproductive
tract. Proc R Soc Lond B
263:369-376.
Bishop JD, Jones CS, Noble LR, 1996. Female control of
paternity in the internally fertilizing compound ascidian Diplosoma
listerianum. 2. Investigation of male mating success using RAPD markers.Proc R Soc Lond B
263:401-407.
Bissoondath CJ, Wiklund C, 1997. Effect of male body
size on sperm precedence in the polyandrous butterfly Pieris napi L.
(Lepidoptera, Pieridae). Behav Ecol
8:518-523.
Briskie JV, Montgomerie R, Birkhead TR, 1997. The evolution of sperm size in birds. Evolution 51:937-945.[Web of Science]
Burley N, 1988. The differential-allocation hypothesis: an experimental test. Am Nat 132:611-628.[Web of Science]
Chapman T, Liddle LF, Kalb JM, Wolfner MF, Partridge L,1995 . Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241-243.[Medline]
Choe JC, Crespi BJ (eds), 1997. The evolution of mating systems in insects and arachnids. Cambridge: Cambridge University Press.
Clark AG, Aguad M, Prout T, Harshman LG, Langley CH,1995 . Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster.Genetics 139:189-201.[Abstract]
Clark AG, Begun DJ, 1998. Female genotypes affect
sperm displacement in Drosophila. Genetics
149:1487-1493.
Crawly MJ, 1993. GLIM for ecologists. Oxford: Blackwell.
Conner JK, 1995. Extreme variability in sperm precedence in the fungus beetle, Bolitotherus cornutus (Coleoptera Tenebrionidae). Ethol Ecol Evol 7:277-280.
Cook PA, Harvey IF, Parker GA, 1997. Predicting variation in sperm precedence. Phil Trans R Soc Lond B 352:771-780.
Cordero C, 1995. Ejaculate substances that affect female insect reproductive physiology and behavior—honest or arbitrary traits? J Theor Biol 174:453-461.
Danielsson I, 1999. Intraspecific variation in sperm precedence in the water strider Gerris lacustris. Behav Ecol Sociobiol (in press).
de Lope F, Møller AP, 1993. Female reproductive effort depends on the degree of ornamentation of their mates.Evolution 47:1152-1160.[Web of Science]
Dewsbury DA, 1982. Ejaculate cost and mate choice.Am Nat 119:601-610.[Web of Science]
Eberhard WG, 1985. Sexual selection and animal genitalia. Cambridge, Massachusetts: Harvard University Press.
Eberhard WG, 1993. Evaluating models of sexual selection: genitalia as a test case. Am Nat 142:564-571.[Web of Science]
Eberhard WG, 1996. Female control: sexual selection by cryptic female choice. Princeton, New Jersey: Princeton University Press.
Eberhard WG, Cordero C, 1995. Sexual selection by cryptic female choice on male seminal products—a new bridge between sexual selection and reproductive physiology. Trends Ecol Evol 10:493-496.
Fairbairn DJ, Preziosi RF, 1994. Sexual selection and the evolution of allometry for sexual size dimorphism in the water strider, Aquarius remigis. Am Nat 144:101-118.[Web of Science]
Harcourt AH, Harvey PH, Larson SG, Short RV, 1981. Testis weight, body weight and breeding system in primates.Nature 293:55-57.[Medline]
Holm S, 1979. A simple sequentially rejective multiple test procedure. Scand J Stat 6:65-70.
Hosken DJ, Stockley P, 1998. Sperm counts.Trends Ecol Evol 13:91-92.
Hughes KA, 1997. Quantitative genetics of sperm precedence in Drosophila melanogaster. Genetics 145:139-151.[Abstract]
Johnstone RA, 1995. Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biol Rev 70:1-65.
LaMunyon CW, Eisner T, 1993. Postcopulatory sexual
selection in an arctiid moth (Utetheisa ornatrix). Proc Natl
Acad Sci USA
90:4689-4692.
LaMunyon CW, Eisner T, 1994. Spermatophore size as
determinant of paternity in an arctiid moth (Utetheisa ornatrix).Proc Natl Acad Sci USA
91:7081-7084.
Lessels CM, Boag PT, 1987. Unrepeatable repeatabilities: a common mistake. Auk 104:116-121.[Web of Science]
Lewis SM, Austad SN, 1990. Sources of intraspecific variation in sperm precedence in red flour beetles. Am Nat 135:351-359.[Web of Science]
Lewis SM, Austad SN, 1994. Sexual selection in flour beetles: the relationship between sperm precedence and male olfactory attractiveness. Behav Ecol 5:219-224.
Lloyd JE, 1979. Mating behavior and natural selection.Fla Entomol 62:17-34.
Massa R, Galanti V, Bottoni L, 1996. Mate choice and reproductive success in the domesticated budgerigar, Melopsittacus undulatus. Ital J Zool 63:243-246.
McCullagh P, Nelder PA, 1989. Generalized linear models. London: Chapman & Hall.
McLain DK, 1980. Female choice and the adaptive significance of prolonged copulation in Nezara viridula (Hemiptera: Pentatomidae). Psyche 87:325-336.
McLain DK, Marsh NB, 1990. Male copulatory success: heritability and relationship to mate fecundity in the southern green stinkbug, Nezara viridula (Hemiptera: Pentatomidae).Heredity 64:161-167.[Web of Science]
Møller AP, 1991. Sperm competition, sperm depletion, paternal care and relative testis size in birds. Am Nat 137:882-906.[Web of Science]
Olsson M, Shine R, Madsen T, Gullberg A, Tegelström H, 1996. Sperm selection by females. Nature 383:585.
Otronen M, 1994. Fertilisation success in the fly Dryomyza anilis (Dryomyzidae): effects of male size and the mating situation. Behav Ecol Sociobiol 35:33-38.[Web of Science]
Otronen M, 1997. Variation in sperm precedence during mating in male flies, Dryomyza anilis. Anim Behav 53:1233-1240.[Web of Science][Medline]
Otronen M, 1998. Male asymmetry and postcopulatory sexual selection in the fly Dryomyza anilis. Behav Ecol Sociobiol 42:185-191.[Web of Science]
Parker GA, 1970. Sperm competition and its evolutionary consequences in insects. Biol Rev 45:525-567.
Parker GA, 1990. Sperm competition games: raffles and
roles. Proc R Soc Lond B
242:120-126.
Parker GA, Simmons LW, 1991. A model of constant random sperm displacement during mating: evidence from Scatophaga. Proc R Soc Lond B 246:107-115.[Medline]
Parker GA, Simmons LW, 1994. Evolution of phenotypic optima and copula duration in dungflies. Nature 370:53-56.
Parker GA, Simmons LW, Kirk H, 1990. Analysing sperm competition data: simple models for predicting mechanisms. Behav Ecol Sociobiol 27:55-65.
Petrie M, Williams A, 1993. Peahens lay more eggs for
peacocks with larger trains. Proc R Soc Lond B
251:127-131.
Pitnick S, 1991. Male size influences mate fecundity and remating interval in Drosophila melanogaster. Anim Behav 41:735-745.[Web of Science]
Preziosi RF, Fairbairn DF, 1996. Sexual size dimorphism and selection in the wild in the water strider Aquarius remigis: body size, components of body size and male mating success.J Evol Biol 9:317-336.[Web of Science]
Rice WR, 1996. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381:232-234.[Medline]
Rowe L, Arnqvist G, 1996. Analysis of the causal components of assortative mating in water striders. Behav Ecol Sociobiol 38:279-286.[Web of Science]
Rowe L, Arnqvist G, Sih A, Krupa JJ, 1994. Sexual conflict and the evolutionary ecology of mating patterns: water striders as a model system. Trends Ecol Evol 9:289-293.
Rubenstein DI, 1989. Sperm competition in the water strider, Gerris remigis. Anim Behav 38:631-636.
Sakaluk SK, Eggert A-K, 1996. Female control of sperm transfer and intraspecific variation in sperm precedence: antecedents to the evolution of a courtship food gift. Evolution 50:694-703.[Web of Science]
Sih A, Krupa JJ, 1992. Predation risk, food deprivation and non-random mating by size in the stream water strider, Aquarius remigis. Behav Ecol Sociobiol 31:51-56
Simmons LW, 1987. Female choice contributes to offspring fitness in the field cricket, Gryllus bimaculatus (De Geer). Behav Ecol Sociobiol 21:313-321.[Web of Science]
Simmons LW, Parker GA, 1992. Individual variation in sperm competition success of yellow dung flies Scatophaga stercoraria. Evolution 46:366-375.[Web of Science]
Simmons LW, Stockley P, Jackson RL, Parker GA, 1996. Sperm competition or sperm selection: no evidence for female influence over paternity in yellow dung flies Scatophaga stercoraria. Behav Ecol Sociobiol 38:199-206.
Smith RL (ed), 1984. Sperm competition and the evolution of animal mating systems. London: Academic Press.
Spence JR, Andersen NM, 1994. Biology of water striders: interaction between systematics and ecology. Annu Rev Entomol 39:101-128.
Svärd L, McNeil JN,1994 . Female benefit, male risk: polyandry in the true armyworm Pseudaletia unipuncta. Behav Ecol Sociobiol 35:319-326.[Web of Science]
Swaddle JP, 1996. Reproductive success and symetry in zebra finches. Anim Behav 51:203-210.
Thornhill R, 1983. Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am Nat 122:765-788.[Web of Science]
Wade MJ, Chang NW, McNaughton M, 1995. Incipient speciation in the flour beetle, Tribolium confusum: premating isolation between natural populations. Heredity 75:453-459.
Ward PI, 1993. Females influence sperm storage and use in the yellow dung fly Scatophaga stercoraria (L.). Behav Ecol Sociobiol 32:313-319.[Web of Science]
Ward PI, Simmons, LW, 1991. Copula duration and testes size in the yellow dung fly, Scatophaga stercoraria (L.): the effects of diet, body size, and mating history. Behav Ecol Sociobiol 29:77-85.
Warner RR, Shapiro DY, Marcanato A, Petersen CW, 1995. Sexual conflict: males with highest mating success convey the lowet fertilization benefits to females. Proc R Soc Lond B 262:135-139.[Medline]
Watson PJ, 1991a. Multiple paternity and first mate sperm precedence in the sierra dome spider, Linyphia litigiosa Keyserling (Linyphiidae). Anim Behav 41:135-148.[Web of Science]
Watson PJ, 1991b. Multiple paternity as genetic bet-hedging in female sierra dome spiders, Linyphia litigiosa (Linyphiidae). Anim Behav 41:343-360.[Web of Science]
Wedell N, 1991. Sperm competition selects for nuptial feeding in a bushcricket. Evolution 45:1975-1978.[Web of Science]
Wedell N, 1996. Mate quality affects reproductive effort in a paternally investing species. Am Nat 148:1075-1088.[Web of Science]
Wedell N, Arak A, 1989. The wartbiter spermatophore and its effect on female reproductive output (Orthoptera: Tettigoniidae, Decticus verrucivorus). Behav Ecol Sociobiol 24:117-125.
Williams DA, 1982. Extra-binomial variation in logistic linear models. Appl Stat 31:144-148.
Wilson N, Tubman SC, Eady PE, Robertson GW, 1997.
Female genotype affects male success in sperm competition. Proc R Soc
Lond B
264:1491-1495.
Wirtz P, 1997. Sperm selection by females.Trends Ecol Evol 12:172-173.
Zeh JA, Zeh DW, 1996. The evolution of polyandry I:
intragenomic conflict and genetic incompatability. Proc R Soc Lond
B
263:1711-1717.
Zeh JA, Zeh DW, 1997. The evolution of polyandry II:
post-copulatory defenses against genetic incompatability. Proc R Soc
Lond B
264:69-75.
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