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Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK
Correspondence should be addressed to W V Holt; Email: Bill.holt{at}ioz.ac.uk
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Abstract |
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 Top Abstract IntroductionCurrent needs for sperm...Fertilisation, sperm quality and...What mechanisms may be...Conclusions; implications for...References |
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To achieve fertilisation a spermatozoon must be capable of responding appropriately to external signalling stimuli; those involving protein kinase-regulated flagellar function seem especially influential in governing effects ranging from non-Mendelian inheritance in mammals to sperm chemotaxis in sea urchins. Examination of the elicited responses reveals considerable heterogeneity in all species. Here we propose that this level of heterogeneity is meaningful both in terms of understanding how spermatozoa from some individuals possess fertility advantages over spermatozoa from their rivals in sperm competition, and in that the heterogeneity should be exploitable in the development of more accurate laboratory tests.
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Introduction |
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TopAbstractIntroductionCurrent needs for sperm...Fertilisation, sperm quality and...What mechanisms may be...Conclusions; implications for...References |
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Current needs for sperm assessment technology |
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TopAbstractIntroductionCurrent needs for sperm...Fertilisation, sperm quality and...What mechanisms may be...Conclusions; implications for...References |
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However, semen assessment methods are not the exclusive province of clinical and veterinary andrologists. Fertility effects of new pharmaceuticals must be evaluated, typically in mice, rats and primates, as part of the national and international approval process. At present, the resultant data remain imprecise. Researchers who investigate male reproductive physiology also use a wide variety of sperm evaluation procedures, depending upon context. Typical examples of current interest might involve evaluating sperm quality and fertility after manipulation of spermatogenesis through transgenic and gene knockout treatments, or through experimental exposure to endocrine-disrupting chemicals. The latter experiments are frequently undertaken using a variety of model organisms, including several species of small and rapidly breeding fishes, such as zebrafish and fathead minnow. Fish sperm assessment is also needed in aquaculture research where semen cryopreservation technology is widely used. Currently there is also considerable academic interest in explaining aspects of evolutionary biology through the influence of sperm competition; this body of literature refers to an array of species from several taxonomic groups, especially mammals, birds, fishes and insects. These studies attempt to identify factors that explain why one apparently normal and fertile semen sample is, in fact, more capable of fertilising eggs than another. Few of the semen tests that are currently available are able to provide mechanistic explanations for these phenomena. This particular observation strongly suggests that much useful information about fertility may be gained by looking at whether the spermatozoa that actually achieve fertilisation under these conditions can be distinguished from those that do not.
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Fertilisation, sperm quality and selection |
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TopAbstractIntroductionCurrent needs for sperm...Fertilisation, sperm quality and...What mechanisms may be...Conclusions; implications for...References |
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The last three decades have witnessed the development of a body of theory about sperm competition, which is said to occur when spermatozoa from more than one male have the opportunity to fertilise eggs from a single female during the same fertile period (for reviews see Parker 1970, 1998). Sperm competition thus occurs when several males mate with a polyandrous female. In this situation, the male who can produce the most and best-quality spermatozoa has an advantage over his rivals, and several studies have demonstrated that large testes size, hence a greater sperm production capacity, is a feature of species which exhibit multimale mating systems (see, for example, Harcourt et al. 1981). Social dominance is also a determinant in such mating systems, as age, body weight and behavioural differences influence the relative number of spermatozoa contributed by each of the males.
A number of classic experimental studies of sperm competition have, however, established that paternity is still skewed even if confounding factors such as sperm numbers and insemination timing are eliminated (for review see Dziuk 1996). Elegant heterospermic insemination (HI) experiments with bull, rabbit and pig spermatozoa, where equal numbers of spermatozoa from two or more males are mixed and inseminated in equal proportions, have shown that spermatozoa from individual males can be ranked in order of fertilisation efficacy (Beatty et al. 1969, Stewart et al. 1974, Parrish & Foote 1985, Berger et al. 1996). Such observations strongly suggest that some aspects of sperm quality per se determine fertilisation success. In this context the meaning of the term ‘sperm quality’ remains unclear and controversial, but implies (i) the existence of a positive correlation between sperm phenotypes and the fitness of the offspring that derives from that particular spermatozoon, or (ii) that some spermatozoa simply possess a ‘fertilisation advantage’ over others. The first alternative would seem more satisfactory from an evolutionary point of view as it suggests a mechanism for the natural selection of fitness traits (Birkhead & Pizzari 2002).
Evidence from genetic studies of natural mating strategies and their outcomes seems to support this view. Paternity identification techniques have revealed previously unsuspected levels of extra-pair paternity across many species. Several hypotheses have been developed that attempt to explain the evolutionary benefits that females may derive from such high levels of polyandry (Zeh & Zeh 2001) and sperm competition (Keller & Reeve 1995), most of which are highly relevant to issues of sperm quality assessment. A few of the suggested hypotheses and their proposed biological benefits are noted in Table 1
. Some authors consider that females can somehow assess the genetic quality of spermatozoa from different males and choose those (the ‘good’ sperm or ‘good’ genes) that will confer genetic benefits to their offspring (Yasui 1997). Others have pointed out that females could ‘choose’ spermatozoa with immunologically compatible characteristics (Zeh & Zeh 2001), perhaps based on the major histocompatibility antigen they express. For species with internal fertilisation, these and other hypotheses would imply the existence of subtle but efficient sperm selection mechanisms in the female reproductive tract. As the nuclear genome contained within the sperm head is highly condensed and inaccessible, it is implausible to infer that a DNA-scanning mechanism exists allowing the female reproductive tract to choose between males or between different spermatozoa. The hypotheses linking sperm quality with offspring quality therefore infer another hypothesis, namely that linkage exists between aspects of sperm phenotype and genotype. A number of authors have supported this proposal, especially in terms of sexual selection and antagonism, where the female reproductive tract is considered to undergo evolutionary changes that tend to impede sperm transport, while spermatozoa are under evolutionary counter pressure to overcome these obstacles (Roldan & Gomendio 1999). Pizzari & Birkhead (2002), who recently reviewed this literature, considered that sperm function is influenced by ‘fertilisation efficiency genes’, which provide fertility advantages when needed. This differs subtly from the cryptic female choice models, since there is no overt necessity that fertilisation efficiency correlate with offspring quality.
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What mechanisms may be responsible for sperm selection? |
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TopAbstractIntroductionCurrent needs for sperm...Fertilisation, sperm quality and...What mechanisms may be...Conclusions; implications for...References |
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Sperm motility
Motility is a common feature of spermatozoa throughout the animal kingdom. In aquatic species with external fertilisation the spermatozoa are released into a hostile environment where they typically become activated then survive for a short period; only 1 or 2 min in the case of freshwater fishes. Their encounter with eggs is a matter of probability, many spermatozoa never reaching them at all. Of those that reach the egg only one enters through the micropyle, an opening that permits sperm entry for a brief period (less than 2 min; Linhart et al. 1995). Sperm selection thus operates at several levels in typical external fertilisation systems, the first priority for spermatozoa being the need to reach an oocyte. The presence of numerous spermatozoa in the ejaculate helps with this initial process, and sperm motility (flagellar beat frequency, velocity and flagellar wave morphology) allows the ejaculate to occupy as much water volume as possible, thus increasing the probability of sperm–egg interactions. Sperm longevity after activation also influences fertilising ability. Superior ability to withstand the osmotic stresses of exposure to hypotonic (freshwater) or hypertonic (seawater) environments confers a selective advantage upon spermatozoa and is recognised as determining relative fertility in fishes. Alternative mating tactics and sperm competition mechanisms in fishes have undergone elaborate evolution (for reviews see Stockley et al. 1997, Taborsky 1998), much of it being directed towards producing large sperm numbers and being able to deposit them in the most favourable sites.
More subtle sperm selection occurring near the egg surface involves cell signalling systems: (i) sperm-activating peptides produced by the egg jelly coat of sea urchin eggs, speract and resact, induce sperm chemotaxis (Ward et al. 1985, Cook et al. 1994). Recently Wood et al.(2003) have shown that these peptides induce calcium fluctuations in the flagellum, thereby controlling the vigour and nature of sperm motility; (ii) Yu et al.(2002) have recently shown that trout spermatozoa adhere to the perimicropylar region of the egg surface through specific cell–cell carbohydrate interactions; these activate protein kinase-related signal transduction mechanisms within the sperm head; and (iii) Iwamatsu et al.(1997) found that linear swimming velocity is correlated with the ability of spermatozoa to enter the micropyle, a finding which relates to observations by Creech et al.(1998) that fish sperm velocity increases under the influence of the signalling molecule, nitric oxide, produced by the eggs around the site of sperm entry. In their paper Wood et al.(2003) commented that sea urchin sperm populations are heterogeneous in their response to speract; one subpopulation within the sample of spermatozoa was unable to respond because the calcium concentrations were already high. Fertilisation success would depend significantly upon the relative size of the unresponsive subpopulation.
For species with internal fertilisation, motility is important for sperm transport within the reproductive tract and for egg penetration. Important clues about the relevance of sperm motility to mammalian fertility have come from a series of papers (especially in relation to the t-haplotype mouse; Olds-Clarke & Johnson 1993) about transmission ratio distortion (TRD). This is an effect whereby genetic mosaicism resulting from meiotic recombination during spermatogenesis leads to the development of genetically distinct sperm subpopulations that are either functionally advantaged or disadvantaged with respect to flagellar activity. While spermatozoa with normal flagellar activity are able to cross the utero–tubal junction and enter the oviduct, those spermatozoa with abnormal flagellar function are unable to do so. Mechanistically, TRD in the case of the t-haplotype occurs because the cell signalling cascades that control flagellar function and motility operate incorrectly. The protein kinases controlling flagellar function in these mice are overexpressed and cause abnormal sperm motility; however, those spermatozoa carrying the t-haplotype also possess a t-complex responder gene (Tcr), which corrects the overexpression of the sperm motility kinase gene (smok), and restores normal flagellar action (Herrmann et al. 1999). During meiosis the Tcr co-segregates with the Y-chromosome and causes 95% skewing of the offspring sex ratio in favour of males by promoting unbalanced fertilisation success. This extreme example, which results in non-Mendelian inheritance, is paralleled by non-Mendelian transmission of retinoblastoma in humans (Girardet et al. 2000); TRD, due to defects in sperm motility, has also been detected in transgenic mouse strains carrying a thymidine kinase reporter gene or a gene for angiotensin-converting enzyme (Hagaman et al. 1998).
These data, from what can be viewed as natural sperm competition experiments, provide an intriguing insight into possible mechanisms of sperm selection. They indicate how genetic traits, not overtly reproductive in nature, can be influenced directly by their association with protein kinase-regulated signalling cascades that affect sperm motility. Reproductive skews detected in HI experiments may therefore be partly attributable to similar mechanisms. This suggestion is supported by observations that when porcine sperm populations are activated by bicarbonate (Tajima et al. 1987), a stimulator of adenylyl cyclase and also indirectly of protein kinase A, heterogeneous responses are seen both within single semen samples and between individual boars (Harrison & Holt 2000, Holt & Harrison 2002) (Fig. 1). Subpopulations of boar spermatozoa respond to bicarbonate in different ways; some are quiescent in the absence of bicarbonate but are rapidly stimulated to maximal progressive motility, some are refractory to stimulation, and others lie somewhere in between. From these observations we hypothesise that when ejaculates from two or more boars are mixed within the female reproductive tract, and exposed to naturally occurring bicarbonate, the relative proportions of the most active sperm subpopulations would differ, and the ejaculates with the highest proportion of activated spermatozoa would be advantaged in terms of fertility. This would undoubtedly skew the relative numbers of spermatozoa colonising the oviduct, even if the relative numbers of spermatozoa initially inseminated were the same. The hypothesis is supported by findings that reproductive advantage in HI experiments with boars is correlated with the numbers of accessory spermatozoa attached to the zona pellucida (Stahlberg et al. 2000); these findings indicate that fertilisation advantage occurs as a result of preferential ability to reach the site of fertilisation, the oviduct. Some evidence that selective breeding for high fertility boars in breeding centres is associated with a greater tendency for bicarbonate-induced sperm activation also supports this hypothesis (Abaigar et al. 1999).
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Capacitation, egg recognition and penetration
In many species with internal fertilisation, spermatozoa do not immediately proceed towards the egg surface, but undergo a period of storage within the female reproductive tract. Storage time can vary from a few hours or days to several years, depending on the species (for comparative data on sperm storage see Birkhead & Moller 1993). The mechanisms of interaction between spermatozoa and the female reproductive tract are of considerable interest, partly because of the potential for understanding the way in which the female reproductive tract maintains sperm viability over such prolonged periods (for review see Hunter & Rodriguez-Martinez 2004). At present there are several indications that sperm storage involves selection, including the observation that the mammalian oviduct preferentially stores uncapacitated spermatozoa (Smith & Yanagimachi 1991, Fazeli et al. 1999). In mammals, capacitation is a complex physiological process that involves biochemical, biophysical and metabolic modifications of all parts of the spermatozoon. It results in altered plasma membrane architecture and permeability, modulates flagellar activity and leads to hyperactivation, a state in which spermatozoa exhibit vigorous and high amplitude flagellar beating that is thought to assist penetration through the zona pellucida. One interesting consequence of capacitation is the apparent activation, or unmasking, of receptors that respond to chemical stimuli from oocytes or thermal gradients within the oviduct (Fabro et al. 2002, Bahat et al. 2003). Once the sperm reservoir has been established in the oviduct, only a small proportion of spermatozoa undergo capacitation at any given period. These spermatozoa, which at that point represent a selected population from the original ejaculate, are therefore subjected to further stringent selection; in mammals only about 10% of the capacitated spermatozoa are responsive to these chemotactic or thermotactic signals (Eisenbach 1999), and they remain responsive for a limited period. Although the details of this process are unknown it is clear that this provides yet another potential mechanism, possibly involving sperm membrane olfactory receptors, whereby spermatozoa from different males could compete for access to the oocyte.
A similar situation exists in aquatic species with external fertilisation where selectivity not only involves discrimination between spermatozoa of the same species, but also involves species specificity. Swanson & Vacquier (2002) recently published a comprehensive review showing that reproductive proteins involved in gamete interactions, particularly, but not exclusively, among aquatic species, undergo unusually rapid evolution driven by sexual antagonism and the constant need for sperm selection. One example of a sophisticated mechanism for cryptic female choice and sexual selection occurs in the sea urchin, Echinometra, where one egg prefers to bind a spermatozoon carrying a particular allele of the sperm-surface protein, bindin, while other eggs have little affinity for the same sperm type (Palumbi 1999).
Sperm selection, fertilisation and embryo development
It is evident from the above discussion that the concept of ‘fertilisation efficiency genes’ (Pizzari & Birkhead 2002) is deceptively complex. Whether their environment is the female reproductive tract or water, spermatozoa are subjected to multiple selective processes that ultimately accept few of their number. This process is thought to have resulted in an unusually rapid evolutionary rate among the proteins involved in these processes, regardless of species or taxon. Because multiple steps are required to achieve fertilisation, variability and meiotic assortment among relevant reproductive genes, they provide limitless ways to affect sperm function. The huge numbers of spermatozoa produced by spermatogenesis represent the results of such recombinations, as though males must strive to cover every likely eventuality of the selective process.
The need to produce large numbers of spermatozoa has been regarded as a compensatory mechanism for inevitable errors of DNA replication during spermatogenesis (Cohen 1969). While this seems an attractive and logical hypothesis, advances in methods of DNA assessment do not provide much direct support. There has been a recent upsurge of clinical interest in assessing the quality of sperm DNA and chromatin structure in relation to human infertility, looking especially at aspects such as DNA fragmentation and the occurrence of strand breakage. Several methods of assessing DNA in individual spermatozoa have been developed, which demonstrate the existence of an inverse correlation between defective DNA structure and embryonic survival in humans (see Larson-Cook et al. 2003 and references therein). Although these tests are highly predictive of negative pregnancy outcome in humans, several studies have shown that they are uncorrelated with fertilisation rate. This discrepancy is important within the context of the present discussion because it means that the selection processes for human fertilisation do not screen for the physical quality of DNA. Studies aimed at investigating the effects of cryopreservation in fish (loach, Misgurnus fossilis) spermatozoa (Kopeika et al. 2003) produced data that parallel the human studies. In these experiments, embryonic mortality was significantly increased when cryopreserved, compared with fresh, spermatozoa were used to fertilise eggs. Fertilisation rate was effectively removed as a variable in these experiments by discarding all unfertilised eggs and only monitoring the development of those that had fertilised normally. As cryopreservation is an unnatural process that may physically damage DNA integrity, it is not surprising to find that natural selection systems cannot detect its effects. Similarly, human clinical infertility may often be caused by unnatural factors such as cigarette smoking (Fraga et al. 1996) and anticancer drug treatment.
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Conclusions; implications for sperm quality assessment |
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TopAbstractIntroductionCurrent needs for sperm...Fertilisation, sperm quality and...What mechanisms may be...Conclusions; implications for...References |
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The foregoing discussion has argued that sperm selection is a powerful and universally important process, and that the fertilising spermatozoa are almost invariably subject to various selective processes prior to, during and, occasionally even after, the union of eggs and spermatozoa. Laboratory-based semen quality assessment methods may therefore be most informative when a degree of sperm selection is incorporated. This assertion is supported by studies of sperm penetration through cervical mucus (Aitken et al. 1992, Cox et al. 2002), and therefore the inclusion of a cervical mucus penetration test in the World Health Organisation’s semen assessment manual (WHO 1992) makes considerable sense. Combining sperm selection protocols with other assays, for example acrosomal integrity and morphology, may also increase the effectiveness of tests. Species with external fertilisation would, however, not be amenable to the same simple sperm selection procedures.
In addition to the use of semen assessment tests for estimating fertility, there is an increasing trend towards the use of spermatozoa as response indicators for pharmacological or toxicological tests. In some cases whole animals are subjected to treatments and their spermatozoa are subsequently tested, while in other scenarios the spermatozoa themselves are tested after in vitro exposure to various compounds. Nuclear DNA may be deleteriously affected during spermatogenesis under the treatment regimes used, and therefore there is considerable merit in using tests, such as ‘TUNEL’ or ‘Comet’ assays for the detection and quantification of DNA strand breakage, that examine the sperm nuclear DNA directly. These could also be combined with sperm selection tests. However, computer-assisted sperm motility measurements are also increasingly used because the spermatozoa are sensitive to environmental conditions (Kime et al. 2001). Sperm motility is suppressed in the presence of low concentrations of toxic chemicals such as heavy metals, but as shown in Fig. 2 the responses also reveal the heterogeneity typical of sperm populations. By developing appropriate statistical methods for the analysis of such heterogeneity, bearing in mind that motility is short-lived and undergoes transient changes, it may be possible to increase considerably the sensitivity of such tests by abandoning the approach whereby all sperm responses are measured and averaged.
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and 2 as examples, while it is clear that computer-assisted semen analysis technology can provide sophisticated data about sperm parameters, their significance is best appreciated if the behaviour of individual spermatozoa is considered. Aggregating the data as simple means and variances hides much of the significant information. A common conclusion that emerges from the literature is that, surprisingly, most spermatozoa are not capable of fertilisation. The biological issues behind this phenomenon suggest that if it were somehow possible to distinguish this defective majority from the competent cells, then laboratory tests would become far more effective at predicting fertility outcomes.
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References |
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TopAbstractIntroductionCurrent needs for sperm...Fertilisation, sperm quality and...What mechanisms may be...Conclusions; implications for...References |
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  L. J. A. Garrett, S. G. Revell, and H. J. Leese Adenosine Triphosphate Production by Bovine Spermatozoa and Its Relationship to Semen Fertilizing Ability J Androl, July 1, 2008; 29(4): 449 - 458. [Abstract] [Full Text] [PDF]
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 F. Martinez-Pastor, E. Cabrita, F. Soares, L. Anel, and M. T. Dinis Multivariate cluster analysis to study motility activation of Solea senegalensis spermatozoa: a model for marine teleosts Reproduction, April 1, 2008; 135(4): 449 - 459. [Abstract] [Full Text] [PDF]
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F. Ardon, D. Helms, E. Sahin, H. Bollwein, E. Topfer-Petersen, and D. Waberski Chromatin-unstable boar spermatozoa have little chance of reaching oocytes in vivo Reproduction, April 1, 2008; 135(4): 461 - 470. [Abstract] [Full Text] [PDF]
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S. Immler Sperm competition and sperm cooperation: the potential role of diploid and haploid expression Reproduction, March 1, 2008; 135(3): 275 - 283. [Abstract] [Full Text] [PDF]
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 T. R. Dreszer, G. D. Wall, D. Haussler, and K. S. Pollard Biased clustered substitutions in the human genome: The footprints of male-driven biased gene conversion Genome Res., October 1, 2007; 17(10): 1420 - 1430. [Abstract] [Full Text] [PDF]
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A M Petrunkina, D Waberski, A R Gunzel-Apel, and E Topfer-Petersen Determinants of sperm quality and fertility in domestic species Reproduction, July 1, 2007; 134(1): 3 - 17. [Abstract] [Full Text] [PDF]
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I. N. Martinez, J. M. Moran, and F. J. Pena Two-Step Cluster Procedure After Principal Component Analysis Identifies Sperm Subpopulations in Canine Ejaculates and Its Relation to Cryoresistance J Androl, July 1, 2006; 27(4): 596 - 603. [Abstract] [Full Text] [PDF]
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