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Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield S10 2TN, UK
Correspondence should be addressed to S Immler; Email: s.immler{at}sheffield.ac.uk
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Abstract |
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 Top Abstract Sperm competitionSperm cooperationHaploid gene expressionHaploid versus diploid gene...Empirical evidence for sperm...Conclusions and future...AcknowledgementsReferences |
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Sperm competition |
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TopAbstractSperm competitionSperm cooperationHaploid gene expressionHaploid versus diploid gene...Empirical evidence for sperm...Conclusions and future...AcknowledgementsReferences |
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One possible reason for the gaps in our understanding of the function of certain sperm traits is that most theoretical and empirical approaches to sperm competition assume that sperm of one male act as a functional entity, similar to somatic tissue cells forming an organ. However, the fundamental difference between somatic cells and sperm is that somatic cells are genetically identical copies of each other resulting from mitosis, whereas sperm are genetically independent haploid units resulting from the processes of meiosis. The genetic variation among sperm of one male (hereafter, referred to as sibling sperm) may have important consequences for the evolution of sperm shape and function, three of which are: (i) sibling sperm are not necessarily all phenotypically identical if the haploid set of genes has any influence on the evolution of sperm shape and function (Joseph & Kirkpatrick 2004). (ii) Genetic differences among sibling sperm imply that sperm of one male compete against each other for the fertilisation of eggs (Parker & Begon 1993, Haig & Bergstrom 1995). (iii) Finally, haploid and diploid gene expression may have diverging effects on the evolution of sperm shape and function, as the diploid male's interests are not necessarily congruent with the haploid sperm's interests resulting in a potential conflict of interest between male and sperm (Reiss 1987, Parker & Begon 1993, Haig & Bergstrom 1995). Empirical evidence for the relative importance of diploid and haploid expression for sperm design and function is increasing (Joseph & Kirkpatrick 2004), and it is clear that haploid gene expression and differential shape and function among sibling sperm are of importance in the context of post-copulatory sexual selection: from the male's point of view, any of its sperm may fertilise the egg as long as it is its own, whereas sibling sperm will compete among each other (Parker & Begon 1993).
The three arguments listed above are of particular relevance in situations referred to as ‘sperm cooperation’, where sperm appear to ‘cooperate’ to increase a male's fertilisation success (e.g. Sivinski 1984, Hayashi 1998, Moore & Moore 2002, Moore et al. 2002). The likelihood that ‘sperm cooperation’ will evolve is affected by the fact that sperm are genetically independent units and different both from each other and from the male that produces them. In this review, the potential for ‘sperm cooperation’ to evolve in response to post-copulatory sexual selection is discussed. First, ‘sperm cooperation’ is defined and then the potential conflict of interest between haploid and diploid gene sets is discussed. Finally, the literature for empirical evidence of sperm cooperation in light of the definitions in earlier sections is reviewed and the potential costs and benefits of sperm cooperation are discussed.
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Sperm cooperation |
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TopAbstractSperm competitionSperm cooperationHaploid gene expressionHaploid versus diploid gene...Empirical evidence for sperm...Conclusions and future...AcknowledgementsReferences |
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The potential for sperm cooperation to evolve depends on the relative importance of diploid and haploid gene expression. If we exclude the potential influence of the male for now, and assume that haploid gene expression is unlimited, sperm cooperation may evolve with the same likelihood as the cooperation between full siblings (Hamilton 1964). The reason for this is that sibling sperm share 50% of their genes, which is the same relationship as between full siblings and therefore, sperm cooperation will occur if the benefits outweigh the costs (Hamilton 1964). However, the situation becomes more complex when the male is included in the scenario, as two parties are involved, and costs and benefits to both of them have to be evaluated. It will depend on the balance between costs and benefits to the haploid sperm on one side and the diploid male on the other side. It has to be pointed out that sperm share 100% of their genes with the male (but the male shares only 50% of its genes with the sperm due to its diploid set of chromosomes) and hence this will increase the likelihood of sperm cooperation to evolve. In addition, haploid gene expression might not be unlimited and hence lower the threshold for sperm cooperation to occur.
Benefits of sperm cooperation include an increase of fertilisation success for both sperm and male in competition with rival sperm or males and therefore, benefits are congruent for both sperm and the male. However, the costs may differ relatively for sperm and for the male: from empirical evidence, it appears that sperm cooperation often involves the loss of fertilisation capability of some sperm (e.g. Moore & Moore 2002, Moore et al. 2002, Till-Bottraud et al. 2005). In this case, the costs are potentially much higher for sperm than for the male: sperm destroy themselves for the benefit of sibling sperm (=costs are 100%), whereas the male loses a certain amount of sperm, yet even if sperm production is costly, the cost to the male is relatively small compared with the cost to the sperm. This discrepancy between the relative cost to sperm and to the male may cause a conflict of interest, since sperm are genetically different from the male.
As outlined above, sperm cooperation will evolve if selective pressures are strong enough, but which are possible selective pressures? Post-copulatory sexual selection including both sperm competition and cryptic female choice may be a potent selective force favouring cooperating sperm and selecting against individually performing sperm. Two theoretical approaches have shown that the evolution of the differentiation of sperm shape and function among sibling sperm in response to post-copulatory sexual selection is possible (Kura & Nakashima 2000, Holman & Snook 2006). One model showed that a ‘soldier sperm class’ may evolve where certain sperm attack rival sperm by potentially destroying themselves (Kura & Nakashima 2000). Similarly, a subsequent model showed that sperm heteromorphism may evolve if non-fertilising sperm protect fertilising sperm from female spermicide (Holman & Snook 2006). The next step is to test these ideas empirically.
In the context of post-copulatory sexual selection and of sperm competition in particular, one question that needs to be addressed is: how can it be avoided that sperm of rival males cheat, for example, by joining cooperating sperm of rival males to obtain some fertilisations? There are several possible solutions to this dilemma: (i) sperm cooperation has evolved entirely in response to cryptic female choice and hence the competition with rival males can be ignored and the risk of being exploited is non-existent; (ii) the cooperating units may be formed before ejaculation and are impenetrable to rival sperm when entering the competition; (iii) cooperating units form fast enough and have terminated their formation before the female copulates with the next male or (iv) sperm are capable of recognising sibling sperm, for example, by a green beard effect (Moore et al. 2002), although there is no evidence for the latter so far.
The evolution of sperm cooperation largely depends on the relative importance of diploid and haploid gene expression and in consequence on the role of the genetic variation among sibling sperm. In the next two sections, the empirical evidence from the point of view of both the haploid sperm and the diploid male is explored.
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Haploid gene expression |
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TopAbstractSperm competitionSperm cooperationHaploid gene expressionHaploid versus diploid gene...Empirical evidence for sperm...Conclusions and future...AcknowledgementsReferences |
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A crucial question is how genetically varied sperm of one male are. Without any recombination, maximum variation of sperm genotypes is directly linked to the number of chromosomes of a species and their combinations. However, recombination processes during meiosis increase the genetic variation among sperm considerably and there is some evidence that recombination rate has an influence on the number of sperm produced (Cohen 1967, 1973). This association between recombination rate and sperm number is thought to be based on the fact that sperm haplotypes exhibit varying quality and to make sure that every haplotype is produced at least once, more sperm have to be produced with increasing recombination rate (Manning & Chamberlain 1994). But how important is this variation in haplotypes among sibling sperm for sperm function?
In mammals, for example, transcription in haploid male germ cells is substantial (Dadoune et al. 2004) and given that after meiosis the haplotype of each sperm is different, sperm may vary in shape and function. However, it is known that cytoplasmic bridges between spermatids during spermiogenesis appear to allow the sharing of haploid gene transcripts and proteins (Dadoune et al. 2004), which would offset the relative importance of haploid gene sets of individual sperm. The fact that transcription is shared during spermiogenesis suggests that at least sperm of one ‘generation’ are phenotypically identical. Yet, there is increasing evidence that gene expression continues even in mature sperm which may lead to functional differences between sperm. Protein translation has been demonstrated in mature mammalian sperm after ejaculation until the moment of fertilisation (Gur & Breitbart 2006). In addition, the presence and the considerable variety of mRNA found in bovine sperm suggest that gene expression in mature sperm may play an important role for sperm function (Gilbert et al. 2007), and that genetic differences in haploid sperm may cause functional differences.
Cytoplasmic bridges between haploid spermatids seem to be particularly important, for example, for proteins encoded on X and Y chromosomes that are known to determine sperm function (Capel et al. 1993, Hendriksen et al. 1995, Moss et al. 1997, Turner et al. 1998, Westbrook et al. 2000). The genetic difference between X and Y sperm is an extreme example for variation in the haploid gene set between sperm. As mentioned above, the cytoplasmic bridges are likely to buffer most of the phenotypic differences between the X and Y sperm. However, there is some evidence that in humans, X sperm are larger than Y sperm (Cui & Matthews 1993, Cui 1997). Furthermore, it appears that in bovine sperm, X and Y sperm differ in some motility parameters linked to sperm head movements but not in swimming velocity parameters (Penfold et al. 1998). The mechanisms causing these differences between X and Y sperm are not known and need to be investigated further.
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Haploid versus diploid gene expression: conflict of interest? |
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TopAbstractSperm competitionSperm cooperationHaploid gene expressionHaploid versus diploid gene...Empirical evidence for sperm...Conclusions and future...AcknowledgementsReferences |
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Meiotic drive by manipulation of sperm function can be found in different taxonomic groups. The male drive in the mosquito Aedes aegypti, for example, induces gamete dysfunction through a range of male distorter chromosomes mainly by the breakage of the X during meiosis, which results in disintegrated sperm organelles (Wood & Ouda 1987, Wood & Newton 1991). Similarly, the X chromosome drive in some Drosophila species is based on the degeneration of Y-bearing sperm in males carrying sex-ratio chromosomes (Hauschteck-Jungen & Maurer 1976). In the fungi Neurospora, spore killers affect half of the meiotic products rendering the spores infertile (Turner & Perkins 1979, 1991), and in the house mouse Mus musculus, a variant of chromosome 17 called the t-haplotype causes segregation distortion where only t-carrying sperm are actually functional whereas+-carrying sperm are immotile (Olds-Clarke & Peitz 1985, Seitz & Bennett 1985). The effects of the haplotypes on sperm function may be deleterious to the male as it results in a significant reduction of functional sperm. First, it is costly for males to produce sperm and the production of malfunctional sperm may be a waste of energy (Preston et al. 2001, Wedell et al. 2002). Secondly, the production of malfunctional or variably functional sperm may be disadvantageous in sperm competition if the rival sperm are all fully functional (Calhim et al. 2007). Lyttle (1991), therefore, suggested that segregation distortion mainly occurs in monogamous species. However, neither the house mouse nor the Drosophila species with segregation distortion are necessarily monogamous: most of the species exhibit female multiple mating and sperm competition (Dean et al. 2006, Holman et al. 2008). The quantification of the potential conflict of interest between the sperm and the male caused by diverging selection between the diploid and the haploid life phases might therefore be an interesting topic for future studies.
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Empirical evidence for sperm cooperation |
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TopAbstractSperm competitionSperm cooperationHaploid gene expressionHaploid versus diploid gene...Empirical evidence for sperm...Conclusions and future...AcknowledgementsReferences |
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The extreme case of phenotypic and functional variation among sibling sperm is sperm heteromorphism, where a male's ejaculate contains fertile and non-fertile sperm, and which is found in different phyla including plants, arthropods, molluscs and vertebrates (Snook 2005, Till-Bottraud et al. 2005). Sperm heteromorphism may reduce the competition among sibling sperm due to the clear division of labour between fertilising and non-fertilising sperm, which may differ considerably in shape and function. The evolution of sperm heteromorphism in the context of post-copulatory sexual selection has been intensely studied in insects, fish and molluscs and has been reviewed in detail elsewhere (e.g. Silberglied et al. 1984, Swallow & Wilkinson 2002, Till-Bottraud et al. 2005). In summary, non-fertilising sperm have been thought to (i) be non-adaptive, (ii) provide nutrients for the receiving female or her eggs, (iii) facilitate transport and/or capacitation of fertilising sperm, (iv) play a role in sperm competition by offending rival sperm, or occupy space to inhibit rival sperm from entering the female sperm storage organs, (v) protect fertilising sperm against female spermicide and (vi) influence cryptic female choice (as found in Holman & Snook 2006). Whereas sperm heteromorphism is well recognised in insects, it is less well studied in other taxa. In an externally fertilising fish, the marine sculpin Hemilepidotus gilberti, for example, it appears that non-fertile sperm act as an obstacle for sperm of rival males by forming clumps that appear to impede sperm of rival males in reaching the eggs (Hayakawa et al. 2002a, 2002b). In the prosobranch, Goniobasis laqueata eusperm get entangled in the tails of the parasperm so that they cannot disperse and reach the eggs (Woodard 1940). In sperm heteromorphic tubificine worms, two types of sperm aggregate, with the non-fertilising sperm forming a sheath around the fertilising sperm for locomotion (Ferraguti et al. 1988, Ferraguti & Ruprecht 1992, Boi et al. 2001; Fig. 1F).
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In contrast to the well-studied phenomenon of sperm heteromorphism, the function of sperm groups in post-copulatory sexual selection has received relatively little attention. This is surprising given the fact that sperm grouping has been described in a wide range of taxonomic groups as diverse as arthropods, chordates and vertebrates (Dujardin 1837, Gray 1928, Phillips 1970, 1972, Dallai & Afzelius 1984, Jamieson 1987, Moore et al. 2002; Fig. 1A–E). There is some evidence that sperm groups may be advantageous in post-copulatory sexual selection. In the fishfly Parachauliodes japonicus, for example, it has been shown that larger bundles containing more sperm reach the sperm storage organs faster than smaller bundles (Hayashi 1998). Sperm pairing occurs in all American marsupials (except one) but not in Australasian marsupials (Temple-Smith 1987; Fig. 1I). Sperm pair inside the male by aligning their morphologically adapted heads precisely and fusing together (Taggart et al. 1993). Phillips (1970) suggested that the function of sperm pairing in marsupials might offer protection for the acrosome during the passage through the male and female reproductive tracts. However, it has been shown that sperm pairs show increased thrusting force that allows them to reach the site of fertilisation, which is not achieved by individual sperm (Moore & Taggart 1995, Moore & Moore 2002). In the European woodmouse Apodemus sylvaticus, sperm form ‘trains’ by interlocking at their heads and flagella, which swim faster and were found to have increased thrusting force compared with individually moving sperm (Moore et al. 2002; Fig. 1H). The hook-shaped sperm head typical of most murine rodents suggests that sperm cooperation may be more widespread than assumed so far (Immler et al. 2007; Fig. 1G). Sperm groups have also been observed in the Norway rat Rattus norvegicus, where sperm form groups by attaching their heads, which results in increased swimming velocity compared with individual sperm (Immler et al. 2007). By contrast, in the house mouse Mus musculus, the sperm groups are slower than the individual sperm (Immler et al. 2007); however, it might be the combination of swimming velocity and increased thrusting force that results in increased fertilisation success. In the Norway rat and the house mouse, thrusting force in viscous media still needs to be tested. Finally, in monotremes, sperm form groups of up to 100 that move forward nearly three times as fast as individual sperm (Jones et al. 2007).
The costs of sperm grouping are less easy to identify than the costs of sperm heteromorphism as the formation of groups differs among taxonomic groups ranging from the direct attachment of sibling sperm by fusion of the membrane (Phillips 1970, 1972) to the conjugation of sperm by a mucous substance (Jamieson 1987). Where sperm attach to each other, separation prior to fertilisation may damage some sperm, rendering them infertile (Phillips 1970, 1972, Moore et al. 2002). In these cases, costs will be relative to the amount of sperm being damaged during the cooperative process. In the American marsupials, for example, sperm pairing results in the destruction of one sperm during separation, which causes the loss of fertilisation capacity of 50% of the sperm. In species where sperm are not damaged during cooperation, costs will be reduced to the production of glycoproteins and similar sticky substances to glue the sperm together (Dallai & Afzelius 1984). The relative costs to both the sperm and the male need to be identified and quantified in more detail.
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Conclusions and future directions |
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TopAbstractSperm competitionSperm cooperationHaploid gene expressionHaploid versus diploid gene...Empirical evidence for sperm...Conclusions and future...AcknowledgementsReferences |
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The study of sperm cooperation and haploid gene expression in the context of post-copulatory sexual selection is still at an early stage and there are many gaps to be filled. The main aims are to identify the costs and benefits of sperm cooperation for both the male and the sperm. Traits that are potentially advantageous in post-copulatory sexual selection have been identified in some cases, such as protection inside the female (L Holman & RR Snook, unpublished data), ‘cheap fillers’ to female copulation delay (Cook & Wedell 1999), inhibitors of rival sperm (Hayakawa et al. 2002a,b), increased swimming velocity and thrusting force of sperm groups (Hayashi 1998, Moore & Moore 2002, Moore et al. 2002, Immler et al. 2007). In contrast, the costs of sperm cooperation are still poorly understood and should be subject to future studies both from a comparative point of view as well as the variation within species.
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Acknowledgements |
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TopAbstractSperm competitionSperm cooperationHaploid gene expressionHaploid versus diploid gene...Empirical evidence for sperm...Conclusions and future...AcknowledgementsReferences |
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Received 27 October 2007
Revision received 4 December 2007
Accepted 10 January 2008
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TopAbstractSperm competitionSperm cooperationHaploid gene expressionHaploid versus diploid gene...Empirical evidence for sperm...Conclusions and future...AcknowledgementsReferences |
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