Behavioral Ecology Vol. 12 No. 6: 726-731
© 2001 International Society for Behavioral Ecology
Sperm size of African cichlids in relation to sperm competition
a Department of Psychology, McMaster University, Hamilton, Ontario L8S 4K1, Canada b Department of Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada c Department of Zoology, Tel Aviv University, Ramat Aviv 69978, Israel
Address correspondence to S. Balshine. E-mail: sigal{at}mcmaster.ca .
Received 29 June 2000; revised 24 November 2000; accepted 24 February 2001.
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ABSTRACT |
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We compared pairs of closely related taxa of cichlid fishes from Lake Tanganyika to examine the relationship between sperm size and the presumed intensity of sperm competition. In contrast to previous reports of relatively short sperm in polygamous fishes across a variety of taxa, we found that polygamous cichlids had significantly longer sperm than their closest monogamous relatives. In addition, sperm length was significantly related to relative testis size (controlling for body size and phylogeny). The site of fertilization may also be correlated with sperm length, as species that fertilize in the female's buccal cavity had significantly shorter sperm than those that fertilized eggs on the substrate. Assuming that relatively large testes and polygamous mating are indicative of more intense sperm competition, these results indicate that sperm length is related to the intensity of sperm competition in this clade of cichlids, as has been found previously in insects, birds, and mammals.
Key words: Cichlidae, Lake Tanganyika, mating systems, sperm competition, sperm morphology, testes.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Ever since Parker (1970
)
recognized the importance of sperm competition as an evolutionary force, many
models that predict the effects of sperm competition on male anatomy,
physiology, and behavior (for a review, see
Parker, 1998) have received
convincing empirical support (for a review, see
Birkhead and Møller,
1998). For example, males in polygamous species are expected to
suffer more sperm competition than their monogamous counterparts, so
polygamous males are predicted to have larger testes relative to their body
size (Parker, 1982,
1990a,b,
1993;
Parker and Begon, 1993), and
empirical studies support this
(Clutton-Brock and Harvey,
1977; Dybas and Dybas,
1981; Harcourt et al.,
1981; Kenagy and Trombulak, 1986;
Warner and Robertson, 1978).
Parker
(1990a,b)
also predicted a positive relation between the intensity of sperm competition
and relative sperm production, and this has been found in insects
(Gage, 1994), fishes
(Stockley et al., 1997), birds
(Birkhead et al., 1993;
Møller and Briskie,
1995), and mammals (Gomendio
and Roldan, 1991; Hosken,
1997; Møller,
1989).
In contrast, the relationship between sperm size and the intensity of sperm
competition remains less clear (both theoretically and empirically). Across
taxa, sperm vary enormously in size, more than 10 orders of magnitude
(Chao et al., 1975;
Pitnick et al., 1995). The
theoretical models make different predictions about whether sperm competition
explains this variation. Two models have been explored: the instantaneous
fertilization model for internal fertilizers (internal fertilization occurs at
one particular instant usually some time after mating) and the continuous
fertilization model for external fertilizers (fertilization occurs in a
continuous fashion immediately after mating). Longer sperm are thought to be
faster swimming (but motile for a shorter period;
Gomendio and Roldan, 1991). In
the simplest form of the instantaneous fertilization model, sperm size is not
predicted to be affected by the intensity of sperm competition
(Parker, 1993), whereas in the
continuous fertilization model (appropriate for most externally fertilizing
fish species), sperm size is predicted to increase with sperm competition
intensity (Ball and Parker,
1996). The different predictions are partly due to the fact that
continuous fertilizers are likely to experience a relatively higher degree of
sperm competition because males release sperm simultaneously, and sperm will
race for the available eggs. Therefore, males will want to increase both sperm
number and sperm swimming speed to maximize the number of collisions with
eggs. Longevity will not be important when there is intense sperm competition
because most of the eggs will be fertilized extremely quickly. In contrast, in
internal fertilizers, ejaculates are released sequentially, and most sperm die
before any competition can occur. Thus, the best strategy under high sperm
competition in internal fertilizers is to maximize sperm number and only under
particular circumstances increase longevity
(Parker, 1998).
In contrast to theory, empirical studies of internal fertilizers have found
an increase in sperm size with sperm competition (birds:
Briskie et al., 1997,
Johnson and Briskie, 1999;
primates and rodents: Gomendio and Roldan,
1991; butterflies: Gage,
1994), and a comparative study of externally fertilizing fish
found a decrease in sperm size with the intensity of sperm competition
(Stockley et al., 1997).
However, Stockley et al.
(1997) used data from numerous
literature sources of variable data quality, which may have confounded their
analyses. As a result, their apparently anomalous findings about the relation
between sperm size and the intensity of sperm competition should be
interpreted with caution.
In this study, we used the comparative approach to study how cichlid sperm
size is related to the intensity of sperm competition. Our results are based
on samples we collected in the field. Cichlids are well suited to the
investigation of sperm competition because they have diverse social mating
systems (monogamy, polygyny and polygynandry;
Keenleyside, 1991;
Kuwamura, 1997), among which
the intensity of sperm competition is expected to vary
(Stockley et al., 1997).
Extensive phylogenetic information is also available for this group (for a
review, see Goodwin et al.,
1998). In cichlids, relative male investment in gonads varies
among species, and this, too, has been shown to correlate with the intensity
of sperm competition in a variety of animal taxa
(Harcourt et al., 1981,
Møller, 1989;
Møller and Briskie,
1995; Stockley et al.,
1997).
Female cichlids typically lay eggs on the ground, either in open nests or
in cavities (caves, burrows, or snail shells), and males fertilize the eggs on
the substrate as they are being laid or shortly thereafter. In many
mouth-brooding cichlids, however, the female picks up her eggs in her buccal
cavity before the male fertilizes them. In these species, the male presents
the female with his anal or pelvic fins, which are covered with small spots
similar in color and size to the female's eggs
(Hert, 1989). The female
attempts to pick up these false eggs, and, as she nips the male's fins, he
ejects sperm into her buccal cavity
(Mrowka, 1987). In previous
comparative studies it has been assumed that mouth-brooding cichlids
experience little or no sperm competition
(Stockley et al., 1997).
However, some female mouth-brooding cichlids move from one male's territory to
another, spawning a few eggs with each male and thus collecting several males'
sperm in their buccal cavity within a few minutes
(Hulata et al., 1981;
Kellogg et al., 1998;
Parker and Kornfield, 1996;
Rossiter and Yamagishi, 1997).
Because cichlid sperm remains active for up to 15 min
(Chao et al., 1987), sperm
competition may be intense in these buccal-fertilizing species.
In this study, our aim was to determine whether sperm size is related to
the intensity of sperm competition in a clade of cichlid fishes, as has been
found in other taxa. By restricting our attention to pairs of close relatives
within a single taxon of fishes living in one lake, we attempted to control
for phylogenetic, ecological, and life-history variation that might influence
sperm size, independent of the intensity of sperm competition. Sperm size has
been shown previously to positively correlate with the number of ova in
externally fertilizing species (Stockley
et al., 1996), so we also examined how sperm length is related to
both the number and size of ova produced at spawning. It is not clear why such
correlations might be expected in fishes (see
Stockley et al., 1996).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Data collection
Between January and May 1998 we collected sexually mature males of 21 cichlid species from various locations on the southern tip of Lake Tanganyika, from the Kalambo River to Ndole Bay in Zambia. We focused particularly on species pairs of close relatives with different mating systems (Table 1). Reproductive information was taken from Brichard (1989
), Konings
(1998), Kuwamura
(1997), and Loiselle
(1985).
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To capture male fish, we used handnets and a 10 x 1 m fence net. Females were released immediately, and males were placed in individual collection bags and brought to the surface within 1 h. Sample sizes per species are listed in Table 1. At the surface we measured each specimen's standard length (mm) and body mass (g). Then we anesthetized each male (using MS222), killed them by quickly severing the spinal cord with a scalpel, and carefully removed the testes. All of the species used in this study were abundant in the lake, and no threatened species were killed as part of the study. Testes were placed immediately in 1.5 ml microcentrifuge Eppendorf tubes, fixed in formalin (4%), and brought back to the laboratory. Because the species in our study breed throughout the year, we assumed that all of the males sampled were sexually active.
In the laboratory, we measured testis lengths to the nearest 0.5 mm and wet
masses to the nearest µg with a Cahn C-31 microbalance. Testes were then
slit open, and free milt was distributed on a slide. If free milt was not
apparent, testes were squeezed or scraped and the liquid spread finely with
formalin. The slides were then allowed to air dry before viewing at
400x. Using a video link to a computer with a flat-screen monitor, we
recorded and digitized images of 10 sperm from each slide using NIH Image
(version 1.59 of the public domain NIH Image program developed at the U.S.
National Institutes of Health, available at
http://rsb.info.nih.gov/nih-image). We analyzed 10 sperm from each of the
males in each of the 21 species. Sperm length was measured from the center of
the head to the end of the tail to the nearest 0.01 µm by tracing a
freehand line using NIH Image. We used the center of the head as a point of
reference because the junction between the sperm head and tail was not always
easy to locate. All of the species we studied had small, spherical sperm heads
whose centers were estimated by eye. To prevent observer bias, all
measurements (testes and sperm) were taken without knowledge of the species
identification. Repeatability (see Sokal
and Rohlf, 1995) was high in an analysis of 20 sperm images, each
measured 3 times independently (rI = 0.97).
Data analyses
Our study species were chosen so that we could analyze sperm differences
between pairs of the closest possible extant relatives
(Table 1), thus minimizing the
effect of phylogeny. We took phylogenetic information from a consensus
supertree (Sanderson et al.,
1998) that we compiled for the species used in this study (see
Figure 1). We chose to accept
Kocher et al.'s (1995)
placement of Eretmodinii basal to Lamprologinii, which yielded nine taxon
pairs for our comparisons (Table
1). If we accept instead Nishida's
(1997) placement of
Eretmodinii basal to Trophini (see Figure
1), then eight comparisons are possible, but we find the same
patterns as described below.
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We used Burt's (1989) method
of paired comparisons to examine the relation between mating systems and
reproductive traits. To do this, we paired each available species with its
closest relative that differed in mating system. In three cases, two closely
related species were grouped for comparison with other taxa
(Table 1), and in those cases
we took mean values for the two species in each taxon. Sample sizes are
therefore the number of independent taxon pairs and not the number of species
originally used in the analysis. In all cases, taxon pairs that we compared
also had the same site of fertilization (buccal vs. substrate), so the
analysis by mating system is not confounded by differences due to
fertilization site.
To test relationships between (log-transformed) continuous variables, we
used Comparative Analysis by Independent Contrasts (CAIC; version 2.6.5;
Purvis and Rambaut, 1995).
CAIC is based on methods for comparative analysis of continuous data, as
described by Harvey and Pagel
(1991). This method identifies
contrasts for each node in the phylogeny that exhibits variation in the test
variable. Linear regressions were forced through the origin
(Harvey and Pagel, 1991).
For correlation analyses on raw data (rather than contrasts), measurements were log transformed to normalize distributions and residuals. None of the distributions of log-transformed variables (such as testis size or body size) was significantly different from normal, so we used parametric statistics throughout.
Because we were testing hypotheses based on theory and considerable
empirical evidence, we used directed statistical tests
(Rice and Gaines, 1994) to
increase statistical power. Directed tests are a useful alternative to
one-tailed tests and provide the safeguard that results in the opposite
direction to those predicted (e.g.,
Stockley et al., 1997) can be
interpreted statistically. In our study, sample sizes were often small, so we
particularly wanted to minimize the chance of Type I error by maximizing
power.
For directed tests we followed the recommendations of Rice and Gaines
(1994) and set 
= 0.05,
= 0.04, and 
= 0.01. The resulting directed p values
for the tests we performed are thus 0.625 times the two-tailed p. We
used directed tests when analyzing the relations between sperm length and both
relative testis mass and mating system because both theory and a number of
previous studies have suggested that sperm will be longer when sperm
competition is more intense. Higher sperm competition is expected in species
with relatively large testes and polygamous (vs. monogamous) mating systems.
Thus, a positive relation is also expected between testes size and mating
system.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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There was no difference in body mass between polygamous and monogamous species (paired t test, t = 0.58, p =.58, n = 9 taxon pairs), so body mass did not confound any comparison between mating systems in this study. However, testis mass was significantly and positively correlated with body mass across species (r =.72, p <.001, N = 21 species). Thus, to measure testis mass independent of body size, we used the residuals from the regression of testis mass on body mass. This residual testis mass is functionally equivalent to the gonadosomatic index (GSI = 100 x testes mass/body mass) used in many studies of fish reproductive biology (e.g., Stockley et al., 1997
). As
expected, cichlids with polygamous mating systems had significantly higher
residual testis mass (paired t = 3.12, directed p =.009,
n = 9 taxon pairs) than their closest monogamous relatives
(Table 1). Variation in sperm length among species was greater than that within species (ANOVA, F20, 133 = 40.3, p <.0001, species nested within mating system), with 81% of the variation in sperm length occurring among species. Telmatochromis vittatus had longest average sperm lengths, on average more than twice as long as those of Asprotilapia leptura, which had the shortest (Table 1).
Substrate-fertilizing species had sperm significantly longer than buccal-fertilizing species (t = 3.92, p =.001, n = 8, 13 species; Figure 2a). Even after controlling for significant differences in both relative testis mass (ANCOVA, F1,17 = 6.2, p =.02) and the relation between sperm length and residual testis mass (ANCOVA, F1,17 = 5.5, p =.03) between buccal and substrate fertilizers, the sperm of substrate fertilizers is significantly and about 23% longer (comparing least squares means) than that of buccal fertilizers (ANCOVA, F1,17 = 12.0, p =.003). Unfortunately, neither of these two analyses could be controlled for phylogeny as all the substrate-fertilizing species in Lake Tanganyika come from the same subfamily (the Lamprologinii).
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Sperm lengths of polygamous cichlids were significantly longer than those of their closest monogamous relatives (paired t test, t = 2.62, directed p =.02, n = 9 taxon pairs; Figure 2b). Indeed, in seven of the nine paired comparisons, polygamous species had the longer sperm. The alternative phylogeny showed similar results; sperm lengths of polygamous cichlids were longer (paired t = 2.23, directed p =.04, n = 8 taxon pairs). On average, the sperm of polygamous cichlids (mean ± SE = 23.1 ± 1.35 µm, n = 11 species) were about 10% longer than the sperm of monogamous species (20.9 ± 1.41 µm, n = 10 species). This pattern is also seen within buccal and substrate fertilizers, where in three of four and four of five taxon pairs, respectively, polygamous taxa had the longer sperm (Table 1).
Controlling for phylogeny, the relation between sperm length and residual testis mass was significant and positive (r2 =.17, b = 0.07, F1,19 = 3.81, directed p =.04, n = 20 contrasts; Figure 3). This relation was positive within both buccal (r2 =.07, directed p =.23, n = 12 contrasts) and substrate fertilizers (r2 =.31, directed p =.09, n = 7 contrasts), though neither was significant, and statistical power was low. Thus, sperm appear to be longer when sperm competition is more intense, assuming that both mating system and residual testis mass are reliable indices of sperm competition.
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Stockley et al. (1996) also
found that sperm length in externally fertilizing species was positively
correlated with the number of ova available per spawning event but not with
ovum size. In our study, sperm length was not significantly related to either
the number (r2 =.10, b = -0.04,
F1,17 = 1.84, p =.19, n = 18 contrasts)
or diameter (r2 =.02, b = 0.04,
F1,17 = 0.42, p =.53, n = 18 contrasts)
of ova at spawning, both analyses controlling for phylogeny. Thus, neither
ovum size nor number at spawning would appear to have confounded our analyses
of the relations between sperm length and the intensity of sperm
competition.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We found longer sperm in cichlid fish species with relatively large testes and polygamous (vs. monogamous) mating systems. This positive relation between sperm length and the intensity of sperm competition (as measured by relative testis mass and mating systems) held true even within fertilization-site categories. This is the first study to find a positive correlation between sperm length and the intensity of sperm competition in fishes. Thus, our results support the predictions of the continuous fertilization model discussed in the introduction. This study also adds cichlid fishes to the growing list of taxa in which variation in sperm length is consistent with the theoretical prediction that selection should favor longer sperm when sperm competition is more intense.
Our results contrast with those of Stockley et al.
(1997), who found that fish
species experiencing greater sperm competition have shorter sperm. Nor did we
find any relation between sperm length and the number of ova as reported by
Stockley et al. (1996), though
our sample size was small, and this idea certainly deserves further study.
Unlike Stockley et al. (1997),
we studied only a single family of fishes. By comparing species pairs that
have similar ecologies, morphologies, fertilization sites, and phylogenetic
histories, but different mating systems, we minimized the risk of finding
differences in sperm size that simply reflect differences in life histories.
In addition, our measurements were standardized; all samples were taken in
exactly the same way, and a single researcher (B.L.) measured all the sperm
and testes.
In our comparison of sperm length between mating systems, we controlled for
the site of fertilization by comparing taxon pairs that have the same site of
fertilization. In addition, we compared the two fertilization sites and found
that buccal-fertilizing cichlids had shorter sperm than substrate fertilizers,
making it tempting to suggest that sperm length in these cichlids is also
influenced by the site of fertilization. For example, species that spawn in
calmer waters have longer-lived sperm compared to species living in turbulent
water (Billard, 1987;
Leach, 1997). Sperm may not
have to travel as far if they are ejected into the buccal cavity or may be
less subject to turbulence than those of external fertilizers. However,
because our comparison involves only a few taxa, a larger sample needs to be
investigated before we can conclude that location of egg fertilization and
water currents affect sperm lengths in cichlids. Stockley et al.
(1997) categorized
buccal-fertilizing cichlids as having little or no sperm competition, whereas
our results suggest that sperm competition may occur in this group.
We used both testis size relative to body mass and social mating system as
measures of the intensity of sperm competition. Sperm competition, however,
may vary within social mating systems, as reproductive sneakers may occur
within many socially monogamous species, and in some polygamous species
females may mate with only a single male (Taborsky,
1994,
1998). Indeed, socially
polygamous males may invest more heavily in gonadal tissue per unit body mass
as a tactic to cope with an increased need for either rapid sperm production
or larger sperm reserves rather than sperm competition per se. Ideally, to
separate this hypothesis from that of sperm competition, we would need to have
genetic confirmation of the real relationship between sperm length and mating
success.
Although several studies of sperm morphology have been published (for
reviews, see Gage, 1998;
Jamieson, 1991), much basic
information is lacking. For example, we need more information on how sperm
lengths affect sperm numbers, mortality, velocity, swimming distances, and
swimming direction. To make sense of seemingly contrasting empirical results,
we must establish a clearer picture of how sperm size trades off with other
components of sperm life history. More work is now needed to see if the
pattern we found here holds in other fish taxa and to try to explain the
different pattern we see when looking across taxa.
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ACKNOWLEDGEMENTS |
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We thank Josephine Morley and Barbara Taborsky for help collecting a number of Eretmodus cyanostictus and Tropheus moorii samples, Chris Eckert and Chris Herlihy for their expert advice with the NIH Image program, and David Earn, Paula Stockley, and two anonymous referees for helpful comments and criticism which greatly improved the manuscript. The field work for this study was funded by the Royal Society; the lab work by the Fisheries Society of the British Isles; and the lab equipment by research and equipment grants from the Natural Sciences and Engineering Research Council of Canada.
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