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1 Grupo de Ecología y Biología de la Reproducción, Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), c/Jose Gutierrez Abascal 2, 28006 Madrid, Spain, 2 Department of Conservation Biology, National Zoological Park, Smithsonian Institution, Washington, District of Columbia 20008, USA and 3 Instituto de Investigación en Recursos Cinegéticos (CSIC-Universidad de Castilla-La Mancha-Junta de Comunidades de Castilla-La Mancha), 02071 Albacete, Spain
Correspondence should be addressed to M Gomendio; Email: montseg{at}mncn.csic.es
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Abstract |
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 Top Abstract Male reproductive success in...Red deer mating systemDeterminants of fertility in...Sperm design and sperm...Secondary sexual characters as...Does testosterone mediate the...Male fertility and offspring...Conclusion and perspectivesAcknowledgementsReferences |
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Male reproductive success in natural populations |
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TopAbstractMale reproductive success in...Red deer mating systemDeterminants of fertility in...Sperm design and sperm...Secondary sexual characters as...Does testosterone mediate the...Male fertility and offspring...Conclusion and perspectivesAcknowledgementsReferences |
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The way in which males and females maximise lifetime reproductive success is very different. Females tend to show higher levels of investment in offspring, and for this reason, they have slower reproductive rates (Clutton-Brock 1988). Differences between females in reproductive success are mainly due to differences in offspring mortality. In contrast, males tend to invest less in offspring, their reproductive rates are higher, and their reproductive success is determined mainly by the number of females they are able to fertilise. Differences between males in lifetime reproductive success are, in most species, higher than among females, so selection on males is expected to be intense. Competition between males to mate with females is therefore strong and has led to the evolution of conspicuous traits like ornaments which make them more attractive to females, or weapons which enhance their ability to win agonistic encounters. In many species, females mate with several males, and competition between males to fertilise ova continues after copulation in the form of sperm competition. This selective pressure has favoured the evolution of larger testes, enhanced sperm production (Gomendio et al. 1998), faster swimming sperm (Gomendio & Roldan 1991, Birkhead et al. 1999, Gage et al. 2004) and a higher proportion of sperm ready to undergo changes required for fertilisation (Gomendio et al. 2006a).
Sex differences in reproductive strategies become more exacerbated the greater the asymmetry between males and females in levels of investment in offspring. Most mammals represent an extreme case, since females invest heavily through gestation and lactation, while males do not invest in offspring beyond sperm production. Thus, variation between males in lifetime reproductive success is high, male–male competition is intense, and females may be choosy about mating partners. In mammals with a polygynous mating system, males defend a harem or a territory to gain sexual access to females, and as a consequence, a few males in the population father the majority of offspring in each breeding season (red deer, Clutton-Brock et al. 1988; fur seals, Hoffman et al. 2003). Competition between males to copulate with females has led to the evolution of traits that improve the chances to win agonistic encounters with other males, such as large body size or weapons (Andersson 1994). A great deal of effort has been made to understand how selective forces have shaped behavioural, morphological and physiological traits that enhance male competitiveness before and after copulation (Andersson 1994, Gomendio et al. 1998). However, most of the studies have assumed that every copulation leads to fertilisation and ignored the possibility that males in natural populations may also differ in their fertility. Such view does not take into account that male reproductive success relies ultimately on the ability of his spermatozoa to fertilise.
Over the last years, our research group has undertaken a comprehensive study of natural populations of Iberian red deer (Cervus elaphus hispanicus) to examine if males do differ in fertility rates and, if so, which are the main determinants of male fertility. This species is a good model to examine these issues because it shows strong polygyny, so male fertility may have a considerable impact on reproductive rates within populations; intense sexual selection has led to the evolution of remarkably elaborated sexual ornaments (antlers) and strong sexual dimorphism; and it is a seasonal breeder so males have a limited period of time to fertilise females. In addition, culling of males during the breeding season makes it possible to gain access to large sample sizes, which are representative of the degree of variation found in natural populations. Finally, we have used an experimental approach which makes use of the variation in semen quality found between males in natural populations to artificially inseminate females from a captive population where other variables can effectively be controlled.
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Red deer mating system |
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TopAbstractMale reproductive success in...Red deer mating systemDeterminants of fertility in...Sperm design and sperm...Secondary sexual characters as...Does testosterone mediate the...Male fertility and offspring...Conclusion and perspectivesAcknowledgementsReferences |
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In male–male encounters, males display their antlers presumably to assess their opponents’ strength, and they are used as weapons when males engage in fights. It is known that fighting success influences harem size, which, in turn, is related to copulation success (Clutton-Brock et al. 1982). Antler size is related to the number of calves fathered by males, and it has been assumed that this is exclusively the result of males with large antlers being able to win more fights with other males (Kruuk et al. 2002). The prevalence of sperm competition in red deer populations is currently believed to be limited. Nevertheless, females do not stay in the same harem during the whole breeding season, so they may copulate with several males during a given sexual cycle; this possibility is supported by the fact that red deer males have large testes in relation to their body size when compared with other species from the Cervidae family (Clutton-Brock et al. 1982).
After the breeding season, males and females separate. Females form stable groups of related individuals, while males have rather weak social relationships (Clutton-Brock et al. 1982). In northern Europe, winter is a critical period due to harsh environmental conditions and food scarcity, and mortality is high, particularly among weak individuals or calves which have not grown large enough. Females give birth during spring, so lactation coincides with a period of food abundance. Lactation is costly energetically, and lactating females are less likely to reproduce the following year than non-lactating females. A consequence of sexual dimorphism in body size is that mothers incur higher reproductive costs when raising male calves, since they need to sustain their more rapid growth rates by investing more in lactation.
There are some suggestions in the literature supporting the existence of female choice in red deer (e.g. Lincoln & Guinness 1973) and it has been shown that female red deer choose males on the basis of their roaring performance (McComb 1991). Thus, female mate choice in red deer has been documented, although it has not received enough attention to allow an assessment of its relevance.
In contrast to populations from northern Europe, in the Mediterranean the period of greatest environmental stress and food scarcity is not winter, but the end of the summer and beginning of autumn when the breeding season takes place. It begins after the hot and dry summer and takes place before the rains start. Thus, males have to face the high costs incurred during the breeding season under severe resource limitations. In these populations, males exhibit a flexible mating system so that some males may defend harems, while other males defend territories where food resources are concentrated and which are used by females as feeding sites (Carranza et al. 1995, 1996). Under these conditions, females move freely in their search for food, moving between territories and between harems rather frequently whether they are in oestrus or not (Carranza et al. 1996).
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Determinants of fertility in natural populations |
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TopAbstractMale reproductive success in...Red deer mating systemDeterminants of fertility in...Sperm design and sperm...Secondary sexual characters as...Does testosterone mediate the...Male fertility and offspring...Conclusion and perspectivesAcknowledgementsReferences |
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Because male fertility has been dismissed as a significant component of male reproductive success, few efforts have been made to understand which semen traits determine male fertility in natural populations. In contrast, this issue has received much attention in two other contexts: livestock breeding and human infertility treatment. The economic benefits derived from maximising the efficiency of livestock breeding have led to major efforts to identify which semen trait(s) determine male fertility. Most of the studies have failed to link specific sperm traits to fertility and the results are rather contradictory or inconclusive (Colenbrander et al. 2003, Foote 2003, Rodriguez-Martinez 2003). On the other hand, treatment of human male infertility has led to the search for ejaculate traits that can explain reproductive failures and predict success at assisted conception. These studies have shown that, in the subpopulation of infertile men which seek medical assistance, sperm concentration in the ejaculate, sperm motility, sperm morphology and acrosomal status are some of the semen traits known to influence male fertility among patients (Drobnis & Overstreet 1992, Tesarik 1994). It is unknown, however, if these same traits would account for fertility differences among males in healthy populations.
The difficulty in identifying which semen traits determine male fertility may lie in the fact that efforts have concentrated in two areas which represent opposite extremes. Livestock breeders have been artificially selecting fertile males for many generations, which may have resulted in little variability between males, particularly on those traits more closely linked to fertility. On the other hand, clinical studies have been mainly concerned with the study of a subpopulation of males whose fertility is compromised. Semen traits responsible for such infertility may not be representative of fertility determinants in less biased populations. Thus, these results cannot be readily extrapolated to natural populations of mammals, which are likely to lie somewhere in between these two extremes. In addition, selective processes acting on natural populations are disrupted in both domestic animals and most human populations, so any potential links between semen traits, male fertility and male reproductive success may be absent in these scenarios. In any case, no information is available on the degree of variability in semen traits and male fertility in natural populations.
Fertility in natural populations of red deer
Semen collected from Iberian red deer from natural populations was used to examine the degree of variation in semen traits and relationships between them (Malo et al. 2005a). Relative testes size and the proportion of motile spermatozoa showed a great deal of variation, with the latter showing a range between 0 and 90% (Fig. 1A and B
). These traits may show more variation than others because they are more sensitive to environmental factors. The proportion of normal spermatozoa and sperm swimming velocity showed an intermediate degree of variation (Fig. 1C and D) with the proportion of normal spermatozoa showing a wide range (12–97%) and a skew towards higher values. Finally, the proportion of viable spermatozoa and the proportion of spermatozoa with an intact acrosome showed low levels of variation, with all males showing high values (Fig. 1E and F). These variables may have stabilised at high values because they are so essential for fertilisation that males with lower values have been intensively selected against in natural populations.
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Semen traits were not associated with others to the same extent (Malo et al. 2005a). Sperm production was found to be closely associated with sperm swimming velocity. This finding suggests that males with high fertility in red deer populations have both high sperm numbers and sperm that swim at high speed. The proportion of motile spermatozoa and quality of motility were closely associated with the proportion of normal spermatozoa, an association which has been frequently postulated (Katz et al. 1982), but for which no strong data were available. Finally, sperm viability and acrosome integrity were strongly associated.
Fertility trials were carried out using spermatozoa from males from natural populations to inseminate captive females, keeping sperm numbers constant. Here, we present results with a larger data set than was originally published (Malo et al. 2005a) given that we have been able to add results from further inseminations. Males from natural populations of Iberian red deer vary markedly in their fertility: some males fertilised 24% of the females while others fertilised 70%. Differences in fertility rates between males were strongly related to sperm swimming velocity as well as to the percentage of morphologically normal spermatozoa (Fig. 2A and B). However, the proportion of motile spermatozoa, the proportion of acrosome integrity and the proportion of viable sperm did not show a significant association with fertility.
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First, these results demonstrate that it is possible to identify specific semen traits which determine fertility in natural populations, despite the lack of success when working with domestic species. Second, they show that some of the traits known to determine fertility among infertile human patients, such as acrosome integrity, are not associated with fertility in natural populations because selection has favoured uniformly high values. Third, that sperm traits believed to play an important role exclusively in the context of sperm competition, such as sperm velocity (Gage et al. 2004), are primary determinants of fertility in males from natural populations in the absence of sperm competition. This implies that, among mammals, there may be no specific sperm traits favoured by sperm competition, but rather that the same traits which are important for fertilisation experience an even greater selection under sperm competition.
Our findings suggest that differences in fertility between males may contribute in a significant way to generate differences in reproductive success. It is widely assumed that the large differences in male lifetime reproductive success observed among polygynous mammals, such as red deer, are mainly due to differences in their ability to win agonistic encounters with other males and defend females from other males. Our results suggest that such scenario is incomplete because once a male defends a harem or a territory its ability to fertilise plays an important role in determining his reproductive success.
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Sperm design and sperm swimming velocity |
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TopAbstractMale reproductive success in...Red deer mating systemDeterminants of fertility in...Sperm design and sperm...Secondary sexual characters as...Does testosterone mediate the...Male fertility and offspring...Conclusion and perspectivesAcknowledgementsReferences |
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However, recent efforts to identify which sperm phenotypic traits determine swimming velocity have been unsuccessful (Gage et al. 2002, Birkhead et al. 2005). Mammalian spermatozoa consist of the head, with a nucleus containing the highly compacted male haploid genome, and the flagellum, which is responsible for sperm motility. The flagellum is, in turn, divided into two components: a) the midpiece containing the mitochondria, which are believed to generate, by oxidative phosphorylation, the energy needed for sperm motility, and b) the principal and terminal pieces (also referred to as ‘rest of the flagellum’) whose beat propel the spermatozoon forward (Turner 2003).
We have examined spermatozoa of Iberian red deer from natural populations to test the hypothesis that the shape of the sperm head and the dimensions of the components of the flagellum determine sperm swimming velocity. Sperm dimensions show variation both between and within males (Fig. 3), although variation between males is greater than within males (Malo et al. 2006). This pattern of small variation within males and large variation between males in the size of sperm components agrees with previous studies (Gage et al. 2002, Birkhead et al. 2005).
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Secondly, it has been suggested that the size of the midpiece is an indicator of mitochondrial loading and, therefore, of the amount of energy available to achieve higher swimming speeds (Anderson & Dixon 2002). Our results do not lend support to such hypotheses because activated spermatozoa with shorter midpieces swim faster (Malo et al. 2006). The role of activated motility is to propel the sperm along the female reproductive tract, through barriers such as the cervix and the uterotubal junction, until they reach the oviduct (Suarez 2007). This leaves the question open as to what the energy generated by mitochondria is needed for. One possibility that deserves further study is that oxidative phosphorylation becomes an important source of energy after sperm hyperactivation, a different type of motility which develops later and contributes to the detachment of spermatozoa from the oviductal wall, allows sperm to reach the site offertilisation and penetrate the oocyte coats (Turner 2003).
Thirdly, we tested the hypothesis that the length of the flagellum may be a key determinant of sperm swimming velocity (Gomendio & Roldan 1991), because it is the beat of the flagellum that generates the force that drives the sperm forward and the amplitude of the waveform determines the sperm trajectory (Katz & Drobnis 1990, Turner 2003). We predicted that if the movement of the principal plus terminal piece is what propels the spermatozoon forward, the key factor should be the size of this component in relation to the length of the whole flagellum. We found support for this idea since the greater the proportion of the rest of the flagellum, when compared with total flagellum length, the faster the sperm swim (Malo et al. 2006). This finding suggests that the roles played by the midpiece and the rest of the flagellum should be considered jointly. In addition to the influence that size of the rest of the flagellum may have in generating the force needed for sperm movement, it may also determine the amount of energy generated. Recent studies show that most of the energy required for sperm motility is generated by glycolysis, rather than oxidative phosphorylation (Eddy 2007, Miki 2007). Glycolysis depends on a sperm-specific glycolytic enzyme which is tightly bound to the fibrous sheath (Miki et al. 2004), a cytoskeletal structure that extends along the principal piece of the flagellum (Eddy et al. 2003, Turner 2003, Eddy 2007).
In conclusion, our results show that the main determinants of sperm swimming velocity are the shape of the head and the proportions between the components of the sperm flagellum. Thus, actual swimming speed will be the result of the combined design of different sperm components. The large inter-male variation in sperm design found among natural populations underlies differences in sperm swimming speed, which, in turn, determine differences in male fertility rates. This supports the idea that sperm design is under strong selective pressures given its role in determining male fertilisation success (Roldan et al. 1992).
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Secondary sexual characters as signals of male fertility |
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TopAbstractMale reproductive success in...Red deer mating systemDeterminants of fertility in...Sperm design and sperm...Secondary sexual characters as...Does testosterone mediate the...Male fertility and offspring...Conclusion and perspectivesAcknowledgementsReferences |
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Much attention has been devoted to the benefits derived by females from choosing particular males. Females may obtain direct benefits such as access to territories of good quality, nutrients transferred by the male, and paternal care, all of which are well documented (Andersson 1994). Females could also obtain indirect benefits such as an improvement in the genetic quality of the offspring or the avoidance of genetic incompatibility. The phenotype-linked fertility hypothesis suggests that females would also benefit from choosing males with elaborated sexual ornaments if they maximise the chances of mating with fertile males (Sheldon 1994). According to this hypothesis secondary sexual ornaments would honestly advertise male fertility. In other words, more attractive males should deliver higher quality ejaculates. There have been few attempts to test this hypothesis, which have yielded contradictory results. In birds, several studies have found no relationship between male phenotype and ejaculate quality (Birkhead & Fletcher 1995, Birkhead et al. 1997), while correlations between plumage brightness and testis size have been reported (Merilä & Sheldon 1999). In fish, several studies found negative correlations between secondary sexual characters (or male sexual activity) and ejaculate quality (Liljedal et al. 1999, Pilastro & Bisazza 1999), while others found positive associations (Matthews et al. 1997). Recent studies on guppies have shown that, when ejaculates from rival males compete and sperm numbers are kept constant, more colourful males have higher parentage success than their less conspicuous counterparts (Evans et al. 2003). The competitive advantage of more colourful males is associated with faster swimming and longer lived sperm (Locatello et al. 2006).
It is well established that both sperm production and sperm swimming velocity determine male fertility. We have examined, for the first time in mammals, whether secondary sexual characters signal these semen traits (Malo et al. 2005b). Among ungulates, male red deer possess antlers that are not only large in relation to other species, but also very complex, containing many branches and points; they are often regarded as one of the most extreme cases of exaggeration of secondary sexual characters in the animal kingdom. Antlers have been regarded exclusively as weapons and their size is believed to be important because it enhances male fighting ability. However, the possibility that antlers may signal other male attributes or that female choice may also play a role have not been considered.
To obtain a global measure that would reflect the size and complexity of red deer antlers, we used eight variables which include length of the main beam, length of the branches, three widths of the main beam at different heights and two point counts. All the measures correlate highly significantly with each other, so we obtained an overall measure of antler size and complexity by conducting a multivariate analysis. Similarly, to obtain an overall measure of sperm velocity, we performed a multivariate analysis including six objective sperm motility parameters. This analysis generated a reliable index of sperm velocity. Our findings show that the global estimate of antler size and complexity is significantly associated with both relative testes size and the overall index of sperm velocity (Malo et al. 2005b). Thus, antler size and complexity is an honest indicator of sperm production and of sperm velocity in male red deer, thus providing support for the phenotype-linked fertility hypothesis.
The finding that antlers are honest indicators of both male sperm production and sperm quality raises the question as to who the signal may be addressed to: other males or females? There are four possible benefits for the female that could explain the function of antlers as honest indicators of male reproductive quality. The first possible benefit is infertility avoidance. The available evidence seems to support this hypothesis, since antlers seem to be signalling reproductive traits, which have been shown to determine male fertility, i.e. sperm production and sperm swimming velocity. Secondly, antlers could signal to females a male’s ability to avoid sperm depletion, since there is evidence that males can become sperm limited as a consequence of sperm production costs and sperm expenditure during reproduction (Preston et al. 2001, Wedell et al. 2002). However, sperm depletion is mainly the result of a reduction in the number of sperm available. The fact that antler size and complexity is associated with sperm velocity suggests that signalling sperm depletion may not be the main function of antlers. Thirdly, male antlers advertise ejaculate competitiveness, which determines fertilisation success under sperm competition, although the prevalence of sperm competition in red deer populations seems to be low. Finally, elaborated sexual ornaments could advertise high quality in males, which, in turn, could be associated with better quality sperm; by mating with these males females could improve offspring quality (see for example, Evans et al. 2004). Both antler size (Kruuk et al. 2002) and semen quality are to a certain extent heritable (Humblot & Ducrocq 1996) suggesting that females may also benefit from the inheritance of both traits by their sons. These benefits would be particularly pronounced in species such as red deer in which female reproductive success is strongly influenced by their son’s lifetime reproductive success (Clutton-Brock et al. 1982).
Another possibility which should not be ruled out is that male antlers could also be signalling to other males the ability to avoid sperm depletion and the competitiveness of the ejaculate. In this way, other males could assess not only a male’s fighting ability, but also the chances that if they copulate with the same females their sperm will be defeated. Males could then use this information to decide whether competing with such a male both at the behavioural (fighting) and physiological (sperm competition) level is a good strategy.
These findings reveal a new function for male red deer antlers and suggest that, among mammals, the degree of elaboration of male secondary sexual characters may signal important aspects of male reproductive quality to females and males. Previous studies demonstrated that antler size is related to the number of calves fathered by males and it has been assumed that this is exclusively the result of males with large antlers being able to win more fights with other males (Kruuk et al. 2002). Our findings suggest that males with large antlers could also achieve higher reproductive success through their enhanced ability to win fertilisations both in competitive and non-competitive contexts and the possible preferences shown by females to mate with them.
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Does testosterone mediate the relationship between antler size and semen traits? |
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TopAbstractMale reproductive success in...Red deer mating systemDeterminants of fertility in...Sperm design and sperm...Secondary sexual characters as...Does testosterone mediate the...Male fertility and offspring...Conclusion and perspectivesAcknowledgementsReferences |
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Red deer are seasonal breeders and cast and regrow their antlers every year. In a captive red deer population, testosterone levels remained low during antler growth, increased during antler mineralisation, reached a peak just before the breeding season started and decreased thereafter, similar to previous reports (Suttie et al. 1984, 1995). Thus, although testosterone may control the timing of key events in the antler cycle (such as casting and pedicle growth), the observation that testosterone levels are low during antler growth supports the current view that the presumed positive link between testosterone levels and antler size is mistaken (Price & Allen 2004). In fact, the opposite may be true, at least in red deer, since males treated with antiandrogens grow larger antlers than controls and testosterone reduces antler growth by influencing insulin-like growth factor-I binding, the latter having an important role in antler growth (Suttie et al. 1995). Evidence from natural populations supports this view since no relationship was found between males’ testosterone levels during the breeding season and antler size (Gomendio et al. 2007).
The annual cycle in testosterone levels is mirrored by changes in testes size, as seen in our captive males. During the breeding season, we found that, in natural populations, differences between males in testosterone levels are closely associated with differences in testes size. These findings support the previously reported (Asher et al. 2000, Roelants et al. 2002) relationship between testosterone, testes size and sperm production. Testosterone is needed for normal spermatogenesis and seems to promote cell proliferation and prevent apoptotic cell death (Roelants et al. 2002).
The potential links between testosterone and semen quality are less clear and the pathways through which testosterone could influence sperm morphology, motility, acrosome integrity or swimming velocity are unknown. In our study sample, there is a significant, but weak, relationship between testosterone levels and proportion of normal spermatozoa, which is a determinant of male fertility (M Gomendio, AF Malo, J Garde, ERS Roldan, unpublished data). However, no relationship was found between testosterone and sperm swimming velocity, which has also been identified as a determinant of male fertility.
In conclusion, our results suggest that testosterone is closely associated with testes size and sperm production, but only weakly associated with other variables of semen quality. In addition, we find no relationship between testosterone and antler size. Thus, the traditional assumption that testosterone mediates the relationships between antler size, semen traits and male fertility should be examined in more detail.
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Male fertility and offspring sex ratio |
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TopAbstractMale reproductive success in...Red deer mating systemDeterminants of fertility in...Sperm design and sperm...Secondary sexual characters as...Does testosterone mediate the...Male fertility and offspring...Conclusion and perspectivesAcknowledgementsReferences |
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It has been argued that the lack of robust results among studies on vertebrate sex ratios is due to the constraints imposed by chromosomal sex determination (Maynard Smith 1978). However, the existence of extreme skews in sex ratios found in some birds and mammals shows that chromosomal sex determination is by no means an absolute constraint (e.g. Komdeur et al. 1997).
The Trivers and Willard hypothesis has been applied most often to mothers, who have a strong influence on offspring quality through maternal care, but it can apply to any quality that parents transmit to offspring, which has a differential effect on the reproductive success of sons and daughters. Among birds, male reproductive success is often related to secondary sexual characters, and thus sons of males with large sexual ornaments will be expected to achieve high reproductive success. There is evidence that offspring sex ratios may be adjusted in relation to the attractiveness of the father (Ellegren et al. 1996). Similarly, in mammals offspring sex ratio is influenced by male body mass (Røed et al. 2006). However, it is widely assumed that such manipulation is under female control.
The possibility that males may also facultatively adjust sex ratio has seldom been considered. In mammals, males are the heterogametic sex producing X- and Y-chromosome bearing spermatozoa, which determine the sex of the offspring. Thus, among mammals, males may have more control over mechanisms of sex determination than in other taxa. In mammals, male traits which may have a greater influence on the reproductive success of sons include male fertility.
We tested the hypothesis that more fertile red deer males produce more sons (Gomendio et al. 2006b). Because female effects on sex ratio exist, it was necessary to disentangle male and female effects by designing an experiment which would minimise differences between females while retaining the inter-male variation in fertility rates found in natural populations. Thus, our experimental design was aimed at eliminating several female factors known to influence sex ratios: i) we avoided the possibility that females may bias sex ratio in response to male quality by artificially inseminating females so that they had no direct experience with the males; ii) differences between females in body condition were minimised using a sample offemales which were all in good physical condition, were kept under similar environmental conditions and had access to an unlimited food supply, and iii) all females were inseminated at the same time in relation to ovulation, avoiding the confounding effects of insemination time. In contrast, using sperm collected during the rut from males living in natural populations, we ensured a representative sample of the large degree of variation in male fertility already described.
When the whole study sample is considered, a similar number of male and female offspring were produced. However, differences between males in fertility rates and in the proportion of male offspring produced were large. Male fertility rates ranged between 24 and 70% and the proportion of male offspring between 25 and 72%. More fertile males sired more sons and less fertile males sired more daughters (Gomendio et al. 2006b). Possible relations between sperm traits and offspring sex ratio were examined. There was a significant relationship between percentage of morphologically normal spermatozoa and proportion of male offspring sired per male, but no significant relationship was found between sperm velocity parameters and proportion of male offspring sired (Gomendio et al. 2006b).
Thus, of the two main determinants of male fertility, sperm swimming velocity and the proportion of normal spermatozoa, the latter was found to be associated with sex ratio. This may be because the proportion of normal spermatozoa is more likely to be inherited by sons (Smital et al. 2005) than sperm swimming velocity, which may be influenced to a greater extent by environmental factors (Kilgallon & Simmons 2005). Thus, males with a higher proportion of normal spermatozoa may benefit from producing sons, who will inherit the trait which will increase their fertility and will thus achieve high reproductive success. In contrast, low-fertility males will benefit from producing daughters, who will not inherit their father’s poor ejaculate quality.
There are two possible mechanisms by which males may adjust sex ratio. First, high- and low-fertility males could differ in the proportion of Y-bearing spermatozoa in the ejaculate (Chandler et al. 2002) resulting in biases in sex ratio at birth. Second, differences between males in the competitiveness of X- and Y-bearing spermatozoa could arise through differential expression of genes carried in the sex chromosomes. Such post-meiotic expression of germ line-specific X- or Y-linked genes has been recently demonstrated (Wang et al. 2005). Furthermore, it has been recently shown that males with deletions in the Y chromosome produce Y-bearing spermatozoa with morphological abnormalities, which are less efficient at fertilisation resulting in sex ratio biases toward females (Ward & Burgoyne 2006). Thus, red deer males with low-fertility rates may have a lower proportion of morphologically normal spermatozoa as a consequence of genetic information on the Y chromosome, which would also impair the chances of fertilisation of Y-bearing spermatozoa. On the contrary, males with high-fertility rates may produce more competitive Y-bearing spermatozoa.
Our experimental approach has revealed unexpectedly large differences in fertility rates between males from natural populations when females were artificially inseminated once. Are such differences in male fertility likely to occur in natural contexts? In the wild, low-fertility males have smaller testes and smaller antlers, so it is unlikely that they could compensate by transferring more sperm or by copulating more often with the same female. Thus, the differences in fertility rates found when all females are inseminated with equal sperm numbers are likely to be exacerbated when differences in sperm numbers come into play in natural contexts, and have a profound influence on male reproductive success. There is not enough information to evaluate whether male fertility rates limit female fecundity in natural populations, in other words, whether females suffer fecundity costs when they mate with low-fertility males. When females do not become pregnant in their first oestrus cycle, they come into oestrus again and have the opportunity to mate with different males. Thus, females may avoid fecundity costs by remating with other males. In spite of this, a significant proportion of females in red deer populations do not reproduce each year, and it has been assumed that this is due to the costs of the previous reproductive event or poor environmental conditions. An unexplored possibility is that low male fertility plays a role.
Our findings suggest that mammalian males can manipulate the sex ratio of their offspring, thus creating an unforeseen evolutionary scenario, which includes conflict of interests between males and females. For instance, a fertile male may benefit from producing sons, but the costs of raising a male may be high for females in poor physical condition (Gomendio et al. 1990). This level of conflict may improve our ability to explain biases in sex ratio at birth.
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Conclusion and perspectives |
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TopAbstractMale reproductive success in...Red deer mating systemDeterminants of fertility in...Sperm design and sperm...Secondary sexual characters as...Does testosterone mediate the...Male fertility and offspring...Conclusion and perspectivesAcknowledgementsReferences |
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Acknowledgements |
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TopAbstractMale reproductive success in...Red deer mating systemDeterminants of fertility in...Sperm design and sperm...Secondary sexual characters as...Does testosterone mediate the...Male fertility and offspring...Conclusion and perspectivesAcknowledgementsReferences |
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Footnotes |
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References |
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TopAbstractMale reproductive success in...Red deer mating systemDeterminants of fertility in...Sperm design and sperm...Secondary sexual characters as...Does testosterone mediate the...Male fertility and offspring...Conclusion and perspectivesAcknowledgementsReferences |
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Anderson MJ & Dixon AF 2002 Motility and midpiece in primates. Nature 416 496.[CrossRef][Medline]
Andersson M 1994 Sexual Selection, Princeton, NJ: Princeton University Press.
Asher GW, Berg DK & Evans G 2000 Storage of semen and artificial insemination in deer. Animal Reproduction Science 62 195–211.[CrossRef][Web of Science][Medline]
Birkhead TR & Fletcher F 1995 Male phenotype and ejaculate quality in the zebra finch Taeniopygia guttata. Proceedings of the Royal Society of London. Series B 262 329–334.
Birkhead TR, Buchanan KL, Devoogd TJ, Pellat EJ, Szekely T & Catchpole CK 1997 Song, sperm quality and testes asymmetry in the sedge warbler. Animal Behaviour 53 965–971.[CrossRef][Web of Science]
Birkhead TR, Martinez JG, Burke T & Froman DP 1999 Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proceedings of the Royal Society of London. Series B 266 1759–1764.[Medline]
Birkhead TR, Pellatt EJ, Brekke P, Yeates R & Castillo-Juarez H 2005 Genetic effects on sperm design in the zebra finch. Nature 434 383–387.[CrossRef][Medline]
Bronson FH 1989 Mammalian Reproductive Biology, Chicago: The University of Chicago Press.
Carranza J, García-Muñoz AJ & Vargas JD 1995 Experimental shifting from harem defense to territoriality in rutting red deer. Animal Behaviour 49 551–554.[CrossRef][Web of Science]
Carranza J, Fernandez Llario P & Gomendio M 1996 Correlates of territoriality in rutting red deer. Ethology 102 793–805.[Web of Science]
Chandler JE, Canal AM, Paul JB & Moser EB 2002 Collection frequency affects percent Y-chromosome bearing sperm, sperm head area and quality of bovine ejaculates. Theriogenology 57 1327–1346.[CrossRef][Web of Science][Medline]
Clutton-Brock TH 1988 Reproductive Success, Chicago: The University of Chicago Press.
Clutton-Brock TH & Iason GR 1986 Sex ratio variation in mammals. Quarterly Review of Biology 61 339–374.[CrossRef][Medline]
Clutton-Brock T, Guinness F & Albon SD 1982 Red Deer. Behaviour and Ecology of the Two Sexes. Wildlife Behavior and Ecology, Edinburgh: Edinburgh University Press.
Clutton-Brock TH, Albon SD & Guinness FE 1984 Maternal dominance, breeding success and birth sex ratios in red deer. Nature 308 358–360.[CrossRef][Web of Science]
Clutton-Brock TH, Albon SD & Guinness FE 1988 Reproductive success in male and female red deer. In Reproductive Success, pp 325–343. Ed. TH Clutton-Brock. Chicago: The University of Chicago Press.
Colenbrander B, Gadella B & Stout T 2003 The predictive value of semen analysis in the evaluation of stallion fertility. Reproduction in Domestic Animals 38 305–311.[CrossRef][Web of Science][Medline]
Drobnis EZ & Overstreet JW 1992 Natural history of mammalian spermatozoa in the female reproductive tract. Oxford Reviews of Reproductive Biology 14 1–45.[Medline]
Eddy EM 2007 The scaffold role of the fibrous sheath. In Spermatology, SRF Supplement 65, pp 45–62. Eds ERS Roldan & M Gomendio. Nottingham: Nottingham University Press.
Eddy EM, Toshimori K & O’Brien DA 2003 Fibrous sheath of mammalian spermatozoa. Microscopy Research and Technique 61 103–115.[CrossRef][Web of Science][Medline]
Ellegren H, Gustafsson L & Sheldon BC 1996 Sex ratio adjustment in relation to paternal attractiveness in a wild bird population. PNAS 93 11723–11728.
Evans JP, Zane L, Francescato S & Pilastro A 2003 Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421 360–363.[CrossRef][Medline]
Evans JP, Kelley JL, Bisazza A, Finazzo E & Pilastro A 2004 Sire attractiveness influences offspring performance in guppies. Proceedings of the Royal Society of London. Series B 271 2035–2042.[Medline]
Foote RH 2003 Fertility estimation: a review of past experience and future prospects. Animal Reproduction Science 75 119–139.[CrossRef][Web of Science][Medline]
Froman DP, Feltmann AJ, Rhoads ML & Kirby JD 1999 Sperm mobility: a primary determinant of fertility in the domestic fowl (Gallus domesticus). Biology of Reproduction 61 400–405.
Gage MJG, MacFarlane C, Yeates S, Shackleton R & Parker GA 2002 Relationships between sperm morphometry and sperm motility in the Atlantic salmon. Journal of Fish Biology 61 1528–1539.[CrossRef][Web of Science]
Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB & Parker GA 2004 Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Current Biology 14 44–47.[Web of Science][Medline]
Gomendio M & Roldan ERS 1991 Sperm competition influences sperm size in mammals. Proceedings of the Royal Society of London. Series B 243 181–185.[Medline]
Gomendio M, Clutton-Brock TH, Albon SD, Guinness FE & Simpson MJ 1990 Mammalian sex ratios and variation in costs of rearing sons and daughters. Nature 343 261–263.[CrossRef][Medline]
Gomendio M, Harcourt AH & Roldan ERS 1998 Sperm competition in mammals. In Sperm Competition and Sexual Selection, pp 667–751. Eds TR Birkhead & AP Møller. London: Academic Press.
Gomendio M, Cassinello J & Roldan ERS 2000 A comparative study of ejaculate traits in three endangered ungulates with different levels of inbreeding: fluctuating asymmetry as an indicator of reproductive and genetic stress. Proceedings of the Royal Society of London. Series B 267 875–882.[Medline]
Gomendio M, Martin-Coello J, Crespo C, Magana C & Roldan ERS 2006a Sperm competition enhances functional capacity of mammalian spermatozoa. PNAS 103 15113–15117.
Gomendio M, Malo AF, Soler AJ, Fernandez-Santos MR, Esteso MC, Garcia AJ, Roldan ERS & Garde J 2006b Male fertility and sex ratio at birth in red deer. Science 314 1445–1447.
Gomendio M, Malo AF, Soler AJ, Garde J & Roldan ERS 2007 Testosterone and male fertility in red deer – response. Science 316 981.
Gray EM 1997 Do female red-winged blackbirds benefit genetically from seeking extra-pair copulations? Animal Behaviour 53 605–623.[CrossRef][Web of Science]
Hewison AJ & Gaillard JM 1999 Successful sons or advantaged daughters? The Trivers–Willard model and sex-biased maternal investment in ungulates. Trends in Ecology and Evolution 14 229–234.[CrossRef]
Hoffman JI, Boyd IL & Amos W 2003 Male reproductive strategy and the importance of maternal status in the Antarctic fur seal (Arctocephalus gazella). Evolution 57 1917–1930.[CrossRef][Web of Science][Medline]
Hoogland JL 1998 Why do female Gunnison’s prairie dogs copulate with more than one male? Animal Behaviour 55 351–359.[CrossRef][Web of Science][Medline]
Humblot P & Ducrocq V 1996 Genetic determinism of sperm production in bulls. Contraception Fertility Sexuality 24 617–623.
Jennions MD & Petrie M 1997 Variation in mate choice and mating preferences: a review of causes and consequences. Biological Reviews 72 283–327.[Medline]
Katz DF & Drobnis E 1990 Analysis and interpretation of the forces generated by spermatozoa. In Fertilization in Mammals, pp 125–137. Eds BD Bavister, J Cummins & ERS Roldan. Norwell, MA: Serono Symposia.
Katz DF, Diel L & Overstreet JW 1982 Differences in sperm movement of morphologically normal and abnormal human seminal spermatozoa. Biology of Reproduction 26 566–570.[Abstract]
Kilgallon SJ & Simmons LW 2005 Image content influences men’s semen quality. Biology Letters 1 253–255.[CrossRef][Web of Science][Medline]
Komdeur J, Daan S, Tinbergen J & Mateman C 1997 Extreme adaptive modification in sex ratio of the Seychelles warbler’s eggs. Nature 385 522–525.[CrossRef][Web of Science]
Kruuk EB, Slate J, Pemberton JM, Brotherstone S, Guinness F & Clutton-Brock T 2002 Antler size in red deer: heritability and selection but no evolution. Evolution 56 1683–1695.[CrossRef][Web of Science][Medline]
Levitan DR 2000 Sperm velocity and longevity trade off each other and influence fertilization in the sea urchin Lytechinus variegatus. Proceedings of the Royal Society of London. Series B 267 531–534.[Medline]
Liljedal S, Folstad I & Skarstein F 1999 Secondary sex traits, parasites, immunity and ejaculate quality in the Arctic charr. Proceedings of the Royal Society of London. Series B 266 1893–1898.[CrossRef]
Lincoln GA & Guinness F 1973 The sexual significance of the rut in the red deer. Journal of Reproduction and Fertility 19 475–489.[CrossRef]
Locatello L, Rasotto MB, Evans JP & Pilastro A 2006 Colourful male guppies produce faster and more viable sperm. Journal of Evolutionary Biology 19 1595–1602.[CrossRef][Web of Science][Medline]
Malo AF, Garde JJ, Soler AJ, García AJ, Gomendio M & Roldan ERS 2005a Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biology of Reproduction 72 822–829.
Malo AF, Roldan ERS, Garde J, Soler AJ & Gomendio M 2005b Antlers honestly advertise sperm production and quality. Proceedings of the Royal Society of London. Series B 272 149–157.[Medline]
Malo AF, Gomendio M, Garde J, Lang-Lenton B, Soler AJ & Roldan ERS 2006 Sperm design and sperm function. Biology Letters 2 246–249.[CrossRef][Web of Science][Medline]
Matthews IM, Evans JP & Magurran AE 1997 Male display rate reveals ejaculate characteristics in the Trinidadian guppy Poecilia reticulata. Proceedings of the Royal Society of London. Series B 264 695–700.[CrossRef]
Maynard Smith J 1978 The Evolution of Sex, Cambridge: Cambridge University Press.
Mayr E 2001 What Evolution Is, London: Phoenix.
McComb KE 1991 Female choice for high roaring rates in red deer, Cervus elaphus. Animal Behaviour 41 79–88.[CrossRef][Web of Science]
Merilä J & Sheldon BC 1999 Testis size variation in the greenfinch Carduelis chloris: relevance for some recent models of sexual selection. Behavioral Ecology and Sociobiology 45 115–123.[CrossRef][Web of Science]
Miki K 2007 Energy metabolism and sperm function. In Spermatology, SRF Supplement 65, pp 309–325. Eds ERS Roldan & M Gomendio. Nottingham: Nottingham University Press.
Miki K, Qu W, Goulding EH, Willis WD, Bunch DO, Strader LF, Perreault SD, Eddy EM & O’Brien DA 2004 Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. PNAS 101 16501–16506.
Morrow EH, Arnqvist G & Pitcher TE 2002 The evolution of infertility: does hatching rate in birds coevolve with female polyandry? Journal of Evolutionary Biology 15 702–709.[CrossRef][Web of Science]
Olsson M & Shine R 1997 Advantages of multiple matings to females: a test of the infertility hypothesis using lizards. Evolution 51 1684–1688.[CrossRef][Web of Science]
Parker GA 1998 Sperm competition and the evolution of ejaculates: towards a theory base. In Sperm Competition and Sexual Selection, pp 3–54. Eds TR Birkhead & AP Møller. London: Academic Press.
Pilastro A & Bisazza A 1999 Insemination efficiency of two alternative male tactics in the guppy (Poecilia reticulata). Proceedings of the Royal Society of London. Series B 266 1887–1891.[CrossRef]
Preston BT, Stevenson IR, Pemberton JM & Wilson K 2001 Dominant rams lose out by sperm depletion. Nature 409 681–682.[CrossRef][Medline]
Price J & Allen S 2004 Exploring the mechanisms regulating regeneration of deer antlers. Philosophical Transactions of the Royal Society of London. Series B 359 809–822.
Rodriguez-Martinez H 2003 Laboratory semen assessment and prediction of fertility: still utopia? Reproduction in Domestic Animals 38 312–318.[CrossRef][Web of Science][Medline]
Røed KH, Holand Ø, Mysterud A, Tverdal A, Kumpula J & Nieminen M 2006 Male phenotypic quality influences offspring sex ratio in a polygynous ungulate. Proceedings of the Royal Society of London. Series B 274 727–733.
Roelants H, Schneider F, Goritz F, Streich J & Blottner S 2002 Seasonal changes of spermatogonial proliferation in roe deer, demonstrated by flow cytometric analysis of c-kit receptor, in relation to follicle-stimulating hormone, luteinizing hormone, and testosterone. Biology of Reproduction 66 305–312.
Roldan ERS & Gomendio M 1999 The Y chromosome as a battle ground for sexual selection. Trends in Ecology and Evolution 14 58–62.[CrossRef]
Roldan ERS, Gomendio M & Vitullo AD 1992 The evolution of eutherian spermatozoa and underlying selective forces: females selection and sperm competition. Biological Reviews 67 551–593.[Medline]
Roldan ERS, Cassinello J, Abaigar T & Gomendio M 1998 Inbreeding, fluctuating asymmetry, and ejaculate quality in an endangered ungulate. Proceedings of the Royal Society of London. Series B 265 243–248.[Medline]
Sheldon BC 1994 Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proceedings of the Royal Society of London. Series B 257 25–30.[CrossRef]
Smital J, Wolf J & De Sousa LL 2005 Estimation of genetic parameters of semen characteristics and reproductive traits in AI boars. Animal Reproduction Science 86 119–130.[CrossRef][Web of Science][Medline]
Snook RR 2005 Sperm in competition: not playing by the numbers. Trends in Ecology and Evolution 20 46–53.[CrossRef]
Suarez SS 2007 Interactions of spermatozoa with the female reproductive tract: inspiration for assisted reproduction. Reproduction, Fertility and Development 19 103–110.[CrossRef][Medline]
Suttie JM, Lincoln GA & Kay RN 1984 Endocrine control of antler growth in red deer stags. Journal of Reproduction and Fertility 71 7–15.
Suttie JM, Fennessy PF, Lapwood KR & Corson ID 1995 Role of steroids in antler growth of red deer stags. Journal of Experimental Zoology 271 120–130.[CrossRef][Web of Science][Medline]
Tesarik J 1994 Male Factor in Human Infertility, Rome: Ares-Serono Symposia Publications.
Trivers RL & Willard DE 1973 Natural selection of parental ability to vary the sex ratio of offspring. Science 179 90–92.
Turner RM 2003 Tales from the tail: what do we really know about sperm motility? Journal of Andrology 24 790–803.
Wallen K & Schneider JE 2000 Reproduction in Context. Social and Environmental Influences on Reproduction, Cambridge, MA: The MIT Press.
Wang PJ, Page DC & McCarrey JR 2005 Differential expression of sex-linked and autosomal germ-cell-specific genes during spermatogenesis in the mouse. Human Molecular Genetics 14 2911–2918.
Ward MA & Burgoyne PS 2006 The effects of deletions of the mouse Y chromosome long arm on sperm function – intracytoplasmic sperm injection (ICSI)-based analysis. Biology of Reproduction 74 652–658.
Wedell N 2007 Sperm competition and ejaculate evolution. In Spermatology, SRF Supplement 65, pp 115–135. Eds ERS Roldan & M Gomendio. Nottingham: Nottingham University Press.
Wedell N, Gage MJG & Parker GA 2002 Sperm competition, male prudence and sperm-limited females. Trends in Ecology and Evolution 17 313–320.[CrossRef]
Wildt DE, O’Brien SJ, Howard JG, Caro TM, Roelke ME, Brown JL & Bush M 1987 Similarity in ejaculate-endocrine characteristics in captive versus free-ranging cheetahs of 2 subspecies. Biology of Reproduction 36 351–360.[Abstract]
Zeh JA & Zeh DW 1997 The evolution of polyandry II. Postcopulatory defences against genetic incompatibility. Proceedings of the Royal Society of London. Series B 264 69–75.[CrossRef]
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