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First published online October 19, 2007
Journal of Experimental Biology 210, 3720-3727 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.008417
Sperm release strategies in marine broadcast spawners: the costs of releasing sperm quickly
1 School of Integrative Biology/Centre for Marine Studies, University of
Queensland, 4072, QLD, Australia
2 Lincoln Marine Science Centre, School of Biological Sciences, Flinders
University, 5606, SA, Australia
* Author for correspondence (e-mail: d.marshall1{at}uq.edu.au)
Accepted 17 July 2007
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: fertilisation, polyspermy, sperm competition
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). When males face significant competition for fertilisations
from other males, established sperm competition theory predicts that males
should release as many sperm as possible
(Parker, 1990;
Parker, 1993;
Parker, 1998;
Parker and Ball, 2005). Indeed
across many organisms, in species where sperm competition is more likely,
males have relatively larger testes (Byrne
et al., 2002; Stockley et al.,
1997). The relationship between sperm competition and male release
strategies is driven by the numerical basis of sperm competition: if a male
achieves numerical superiority at fertilisation, it is predicted that he will
sire the highest proportion of eggs (see references above). Whilst the
dynamics of sperm release have been well studied for some organisms, marine
broadcast spawning (the most common form of reproduction in the sea) has
received relatively little attention. This is despite broadcast spawners
representing the ancestral mode of reproduction and their repeated use as a
basis for sperm competition theory (Ball
and Parker, 1996; Williams et
al., 2005), species recognition
(Panhuis et al., 2006) and the
evolution of anisogamy [sperm and eggs of different sizes
(Levitan, 1996;
Levitan and Ferrell,
2006)].
Sperm competition is probably intense for most broadcast spawners. Sperm
limitation (incomplete fertilisation success due to insufficient sperm) may be
common in the marine environment (Levitan
and Petersen, 1995; Yund,
2000), but males rarely, if ever, gain exclusive access to a batch
of eggs and indeed initial studies suggest that broadcast spawning is highly
polygamous (Brockmann et al.,
1994; Levitan,
2004; Levitan,
2005a). Most observations of spawning events show that multiple
individuals spawn, sometimes within a dense aggregation, and therefore
multiple ejaculates of sperm will be competing for a limited pool of eggs
(Hardege and Bentley, 1997;
Lamare and Stewart, 1998;
Marshall, 2002;
Marshall et al., 2004).
Spawning times can be restricted to narrow environmental windows
(Babcock et al., 1986;
Marshall, 2002) and as such,
males are probably unable to `wait' for periods of less intense sperm
competition (Fuller, 1998).
Consequently, much of the theory on sperm competition would predict that in
the presence of many competing ejaculates, broadcast spawning males should
release all their sperm as quickly as possible over a short time scale
(Ball and Parker, 1996;
Stockley et al., 1996).
Current observations of sperm release rates in broadcast spawners do not
support the prediction that broadcast spawning males should release sperm
quickly (Table 1). For a number
of species, males tend to release their gametes more slowly than females
(Table 1). Furthermore, some
species release their sperm in a viscous matrix that further reduces the
advection of sperm from the site of spawning such that sperm slowly wisps away
(Marshall, 2002;
Marshall et al., 2004;
Thomas, 1994). At higher
temporal scales, males repeatedly spawn over successive days rather than
release all their sperm in a single event
(Hardege and Bentley, 1997).
Finally, larger males do not release more sperm than smaller males in any one
spawning event (Hardege and Bentley,
1997; Styan and Butler,
2003). All of these behaviours appear to be contrary to the
predictions of traditional theory concerning sperm competition
(Williams et al., 2005). Why
do broadcast spawning males release sperm slowly when achieving numerical
superiority with sperm should carry a fitness benefit?
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The kinetics of fertilisation in broadcast spawners may account for the
sperm release strategies of broadcast spawning males. In a number of different
marine invertebrate taxa, a few seconds after an egg is fertilised by a sperm,
a `fast' electrical block is formed that prevents additional sperm from fusing
with the egg (Gould and Stephano,
2003; Wong and Wessel,
2006). This first block prevents polyspermy (a lethal condition in
marine invertebrate eggs) but does not prevent sperm from attaching to the
egg. Within minutes of fertilisation a second `slow' or permanent block then
forms, which prevents the attachment of subsequent sperm to outside of the egg
(Gould and Stephano, 2003).
The mechanisms for this change in the attachment properties of the egg vary
among taxa but can involve the retraction of microvilli, the expansion of a
fertilisation envelope, or the release of cortical granules that modify the
surface of the vitteline coat (Gould and
Stephano, 2003). Because we will discuss the speed of onset of
these blocks and use of terms such as `fast, slow blocks' would be confusing,
for clarity, we will refer to these two blocks as `electrical' and
`permanent', respectively, throughout the manuscript.
Given the time taken for fertilised eggs to form the permanent block to
polyspermy, a temporal window exists in which sperm can attach to the egg
surface without achieving fertilisation, and as such eggs can act as `sperm
sinks', removing sperm from the pool without resulting in further
fertilisations. A recent study showed that a single egg could remove up to 140
sperm (Marshall and Evans,
2005b), and therefore eggs that have not formed slow polyspermy
blocks could represent a significant drain on the sperm pool. Here, we test
the hypothesis that faster sperm release rates result in a higher proportion
of sperm being wasted whereas slower release speeds allow sufficient time for
permanent polyspermy blocks to form. Simultaneously, we explore the potential
selection pressures that may have led to the evolution of permanent polyspermy
blocks: why do females have a permanent polyspermy block if the electrical
block is sufficient to prevent polyspermy? If we hope to understand the effect
of permanent polyspermy blocks on the benefits of releasing sperm quickly or
slowly, then we need direct measures of the fertilisation success of males
that release sperm at different rates under hydrodynamic conditions that are
as realistic as possible. We used flume experiments to simulate the fast and
slow release of sperm and compared fertilisation rates across two groups of
eggs on the broadcast spawning marine invertebrate, Galeolaria
caespitosa. We used two groups of eggs because we predicted that any
upstream `wastage' of eggs generated by a fast release speed would result in
decreased fertilisation success downstream. We found that sperm release rates
had dramatic consequences for male fertilisation success and so we further
investigated the time course requirements for the formation of polyspermy
blocks.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Marshall and
Evans, 2005b).
The sperm of G. caespitosa are active immediately upon release
(D.J.M. and T.F.B., personal observation) and remain viable and achieve high
rates of fertilisation for up to 3 h after release
(Ross and Bidwell, 2001). It
is important to note that in G. caespitosa, exposure to eggs or
seawater that has contained eggs (`egg water') does not activate or change the
motility of sperm in this species
(Kupriyanova and Havenhand,
2002).
Flume experiment
The aim of this experiment was to examine the effect of male release speed
on subsequent fertilisation success across two batches of eggs, one batch
downstream from the other. The internal dimensions of the flume were 1500 mm
longx300 mm wide, filled with water to a depth of 80 mm. These
dimensions do not preclude wall effects
(Nowell and Jumars, 1987), but
given that we were principally interested in comparing differences among runs
within the same flume, these effects are unlikely to affect the outcome of our
study. We induced laminar flow in each lane by using a 300 mmx300
mmx200 mm collimator made of drinking straws (see
Yund and Meidel, 2003).
Filtered seawater pumped from Boston Bay was first pumped to a 20-litre,
constant head tank and then gravity fed into the flume. After travelling the
length of the flume, the water exited the flume over a wall 80 mm high (the
flume was non-recirculating). Initial observations using dye suggested that
water flow was laminar across the experimental arena. The current speed within
the flume was kept at a constant 100 mm s–1 [current speed
estimated as described elsewhere (Yund and
Meidel, 2003)]. At the head of the flume, the sperm
(concentration: 
1x108 sperm ml–1) from
3–4 males was released from a 60 ml syringe. To simulate fast release of
sperm, two short bursts of 10 ml each were released within 10 s. To simulate
the slow release of sperm, 12 short bursts were released over 120 s. Thus in
both treatments, a total of 20 ml of sperm was released. Care was taken to
ensure that we used the same rate of plunger depression across the treatments,
so that the sperm in one treatment did not experience different shear forces
to those in the other (Mead and Denny,
1995), but the duration of release differed between the two
treatments. Downstream from the release points were two batches of eggs, each
consisting of eggs spawned from 3–5 females. The proximal batch of eggs
was 200 mm from the sperm release point and the distal batch was 800 mm (both
batches were placed in the longitudinal centre of the flume). To place the
eggs into the flume, we used a syringe to gently release the eggs onto the
surface of the flume. Galeolaria caespitosa eggs are negatively
buoyant and remained in a small `clump' even while water was running through
the flume. We allowed the eggs in both batches to accumulate fertilisations
and then 10 min after sperm release, the eggs were collected using pipettes
and placed into 70 ml polyethylene specimen jars, where they were allowed to
develop for a further 2 h before fertilisation was assessed as in
(Marshall and Evans, 2005a).
We alternated fast release and slow release runs (10 of each) and conducted at
least two runs on any given day. Between each run we drained the flume and
rinsed it with freshwater before refilling.
Laboratory experiments
Our flume experiments indicated that sperm that is released over a longer
period achieves greater fertilisation success in the distal batch of eggs than
sperm that is released over a shorter period (see Results). Previous work on
G. caespitosa has shown that unfertilised eggs deplete sperm
solutions having a ratio of more than one sperm per egg
(Marshall and Evans, 2005b).
We conducted laboratory trials to determine if eggs that had recently been
fertilised had the same sperm depleting effect as unfertilised eggs. To do
this we conducted two experiments. The first compared the effects of
unfertilised eggs and eggs that had been fertilised (for 1, 10 or 30 min) on
the abundance of sperm after 5 min. Our protocol was similar to that described
previously (Marshall and Evans,
2005b) but included additional treatments and some modifications.
We first collected a batch of eggs from three females and split the eggs into
four groups. The eggs in each were diluted in filtered seawater to a final
concentration of 1000 eggs ml–1. The first group of eggs was
exposed to a high concentration (1.5±0.5x106 sperm
ml–1) of (non-focal) sperm from three males for a period of 1
min before being thoroughly rinsed in filtered seawater to remove any sperm
that had not bound to the eggs (the eggs were retained on a 25 µm plankton
mesh filter). We then set this group aside for 10 min. 9 min later, the second
group was exposed as above and set aside for only 1 min. Thus two pre-exposed
groups of eggs were the same age but differed in the length of time for which
they had been allowed to develop after exposure to the non-focal sperm. The
third group of eggs was not exposed to sperm but was rinsed and filtered as in
the other groups. We then took all three batches of eggs (in a 2 ml solution)
and exposed them to 1 ml of sperm from a focal male for 15 min. A fourth vial
containing only 2 ml seawater was also included as a control. The
concentration of sperm was first diluted to a concentration of
(1.5±0.5x106 sperm ml–1). Thus, the
focal sperm from a single male was split into four groups and was exposed to
(i) unfertilised eggs, (ii) eggs that had been fertilised only 1 min earlier,
(iii) eggs that had been fertilised 10 min earlier, (iv) just seawater. For
all of our experiments, the concentration of non-focal sperm was sufficient to
result in >95% fertilisation success in the eggs. We then filtered the eggs
from the solution (the control was treated identically) and estimated the
concentration of focal sperm that remained in solution. We also exposed the
focal sperm to additional `fresh' eggs to assess their fertilisation capacity,
but logistical constraints resulted in us being unable to expose sperm from
the `1 min' treatment to eggs. Consequently, we repeated the above experiments
but had only two treatments: a control, where sperm were exposed to seawater
only, and the `1 min' treatment group of eggs. We then examined the subsequent
fertilisation success of the focal sperm with fresh eggs.
Statistical analyses
We analysed the results of our flume experiment using a two-factor ANOVA
where sperm-release speed and egg position were both fixed factors. To analyse
the results of our laboratory experiment we used a mixed-model, two-factor
ANOVA where focal male identity was a random factor and egg treatment was a
fixed factor. We first ran a mixed model ANOVA including male identity and
treatment; however, there was no interaction between male identity and
treatment (F20,76=0.79, P=0.71) and so it was
removed from the final model (Quinn and
Keough, 2002). To further examine the differences between levels
of the egg treatment, we used incremental planned comparisons
(Quinn and Keough, 2002) and
pooled levels that were not significantly different from each other.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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75% fertilisation success. However, release rate
strongly affected the fertilisation rate of the eggs that were further
downstream with the slow release rate resulting in much higher fertilisation
rates than the fast release rate.
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Exposure of sperm to unfertilised eggs caused an almost 50% reduction in sperm concentration relative to the control (Table 3; Fig. 2). However, exposure to eggs that had been previously exposed to sperm had less of an effect on focal sperm concentrations. Eggs that been exposed to sperm only 1 min before exposure to the focal sperm had no significant effect on the subsequent focal sperm concentration. Subsequent fertilisation rates of eggs fertilised with pre-exposed sperm reflected this pattern. Sperm that had been exposed to unfertilised eggs achieved much lower fertilisation rates than sperm that had been exposed to fertilised eggs or no eggs at all (Fig. 2; F2,12=23.93, P<0.001; Tukey's pairwise comparisons: Control=10 min>unfertilised). Similarly, sperm that had been exposed to recently (1 min) exposed eggs had similar fertilisation rates to sperm that been exposed to no eggs at all (t=0.161, d.f.=10, P=0.875).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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), but shows that the level of depletion depends on the
release rate of males.
Despite the strong research effort devoted to theoretical considerations of
sperm release strategies in external fertilisers
(Parker and Ball, 2005;
Parker, 1982;
Parker, 2000;
Parker et al., 1996;
Parker et al., 1997;
Parker and Begon, 1986;
Parker and Begon, 1993;
Williams et al., 2005),
studies that empirically examine the effects of different male release rates
(over small temporal scales) on subsequent fertilisation success are rare.
Levitan (Levitan, 2005b)
showed strong pre-emption effects in the field with males that access eggs
first having higher fertilisation. Levitan also predicted that releasing sperm
slowly over time may be advantageous when sperm competition is low because it
may increase the likelihood of sperm encountering eggs
(Levitan, 2005b). Our present
results provide further support for this prediction, as releasing sperm slowly
will also decrease sperm `wastage' on nearby females. We believe the next step
in exploring what sperm release strategies should be favoured by broadcast
spawning males is to use game theoretic models, previously developed for a
`generalised external fertiliser' (e.g.
Ball and Parker, 1996), but
with assumptions that are more relevant to broadcast spawners.
The relative benefits of releasing sperm quickly or slowly are likely to
depend on a number of biological factors. The time taken for fertilised eggs
to form the slow block to polyspermy (i.e. cease being sperm sinks) will be
the most important factor, with slower blocks favouring slow sperm release
rates and faster blocks favouring faster release rates. Currently, there are
too few examinations of permanent polyspermy blocks to generalise but at least
for some species, it appears that slower release rates are likely to be
favoured. Our results are probably most relevant for species in which spawned
eggs are negatively buoyant and tend to remain on the substratum during
fertilisation. It is in these species that sperm are most likely to travel
over several groups of eggs. Whilst this is a common mode of reproduction in
broadcast spawners (Marshall,
2002; Marshall et al.,
2004; Meidel and Yund,
2001; Yund and Meidel,
2003), other species such as scleractinian corals release
positively buoyant gametes that are likely to disperse in clouds along with
any released sperm (Babcock et al.,
1986). In such situations, there is still a `leading edge' of eggs
that encounter the sperm first and may rob downstream eggs of sufficient
sperm, but the cloud of gametes will be more diffuse. We can only speculate as
to whether sperm release rates will have similar effects in species such as
these and look forward to future studies.
The likelihood of achieving additional fertilisations downstream from the
nearest female will also strongly affect the relative benefits of a fast or
slow sperm release strategy. If males have a small chance of fertilising
females downstream (either because of sperm dilution effects or pre-emption by
other males) then there will be few benefits of spawning slowly as males can
afford to `waste' all their sperm on the first female. It would be interesting
to determine if the rate at which sperm are released is facultative, adjusted
by spawning males according to local conditions. While females have been shown
to adjust their spawning behaviour according to the proximity of spawning
males (Marshall et al., 2004),
we know of no similar study on males adjusting their release rates in
broadcast spawners. This is despite clear evidence that spawners communicate
information regarding reproduction prior to spawning events
(Hamel and Mercier, 1997;
Hardege and Bentley, 1997).
Male–male competition is likely to be crucial in determining the costs
and benefits of different release strategies in broadcast spawners. Assuming
male fertilisation success operates on a raffle principle in broadcast
spawners, then males with the highest concentration of sperm present should
secure the most fertilisations (Parker et
al., 1996). Thus if there are many females spawning locally, then
a fast release rate might still be favoured because the reduction in
downstream fertilisations becomes less important. However, there are two key
issues that could further affect sperm release strategies: assortative mating
and polyspermy. Several studies now suggest that fertilisation does not
operate according to a raffle principle, rather different combinations of
sperm and eggs are more compatible with each other than others
(Palumbi, 1999;
Evans and Marshall, 2005;
Marshall and Evans, 2005a;
Levitan and Ferrell, 2006).
Initial evidence suggests that these differences in compatibility could affect
the outcome of sperm competition in broadcast spawners
(Levitan and Ferrell, 2006)
and this is likely to affect sperm release strategies in broadcast spawners.
Polyspermy (whereby multiple sperm enter the eggs before a fast block is
formed) will also affect male release strategies
(Bode and Marshall, 2007).
Whilst releasing more sperm should increase a male's local reproductive
success, if other males do the same, overall fertilisation success will
decrease due to polyspermy (Bode and
Marshall, 2007). Thus there are multiple factors that will affect
what is the `best' sperm release strategy, but regardless of these factors,
our study suggests that males that release all of their sperm quickly are not
always going to achieve the highest reproductive success overall.
Our results have some counter-intuitive implications for our understanding
of the evolution of permanent polyspermy blocks. Our flume experiments were
used to examine the effect of sperm release rates on male fertilisation
success. We could have used the same experimental design to examine how the
time for a permanent polyspermy block to form will affect female fertilisation
success. To explain: changing the sperm release rate whilst the permanent
polyspermy block speed stayed constant, from a fertilisation kinetics
perspective, is identical to holding the sperm release rate constant and
changing onset speed of the permanent polyspermy block
(Fig. 3). In both instances,
the total number of sperm that pass over the eggs before a permanent
polyspermy block forms is the only thing that varies. Thus a fast sperm
release rate simulates a slower permanent block and vice versa. From
the perspective of female fertilisation success, therefore, our flume results
show that when sperm concentrations limit fertilisation, eggs with faster
acting permanent polyspermy blocks should have higher fertilisation overall.
This is because, even in a single clutch of eggs, there will be upstream eggs
that access sperm before downstream eggs and effectively `rob' their
(potential) siblings of fertilisations. Any decrease in the time taken for
eggs to become impervious to sperm should reduce the number of sperm that are
wasted by the upstream eggs, thereby enhancing fertilisation success
downstream. However, it should be noted that this prediction will only hold if
the duration of sperm release exceeds the time taken for the permanent
polyspermy block to form, a condition that seems likely
(Table 1). Overall then faster
permanent polyspermy blocks should enhance fertilisation under sperm limiting
conditions. Polyspermy blocks have been cited as evidence that sperm excess
conditions are common in natural populations
(Yund, 2000). We agree, but
suggest that the two types of polyspermy blocks and their selection pressures
should be distinguished. Electrical polyspermy blocks may have evolved in
response to sperm excess but permanent polyspermy blocks may have evolved in
response to sperm limiting conditions. Note that we do not suggest that sperm
limitation is the sole selective pressure that led to the evolution of
permanent blocks; other changes associated with the induction of permanent
blocks may also be important (e.g. egg hardening may protect from physical
stress and pathogens).
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Our laboratory results suggest that in Galeolaria caespitosa, eggs
become impervious to sperm attachment within 1 min of fertilisation. Direct
observations of eggs and sperm further support this suggestion, with
unfertilised eggs having multiple sperm attached whilst recently fertilised
eggs do not (Fig. 4). Studies
examining blocks to polyspermy in polychaetes are rare, but this time course
seems faster than for other species
(Eckberg and Anderson, 1985).
Similarly, sperm attachment can continue for up to 5 min after fertilisation
in other taxa (Gould and Stephano,
2003; Wong and Wessel,
2006). The density of adult Galeolaria caespitosa varies
dramatically in the field and so it is difficult to predict the typical sperm
environment for eggs of this species, but a recent manipulative study suggests
that concentrations in the field will be limiting
(Hollows et al., 2007). That
the onset of the permanent polyspermy block is rapid further supports the
notion that sperm are limiting in the field and there is strong selection
pressure to reduce the number of sperm that are `wasted' by fertilised
eggs.
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A recent review (Wedell et al.,
2002) challenged the notion that sperm are a cheap commodity for
males such that `the word excess has no meaning for males',
highlighting a number of instances of male `prudence' with regards to sperm
release. Our results further support this challenge, whereby males that
release sperm slowly will waste fewer sperm than males that release quickly.
The scarce data on male release rates in the wild further support the notion
that males are `prudent' with regards to sperm release. We suggest that in the
ancestral mode of reproduction, broadcast spawning, sperm release strategies
represent a compromise by which males compete for fertilisations as is the
traditional view, but also minimise sperm wastage.
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Acknowledgments |
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