Red deer antlers have been widely used as an extreme example of exaggerated male secondary sexual characters traits but have always been regarded exclusively as weapons. The fact that males often display their antlers has been interpreted as a display of fighting ability and the possibility that antlers may signal other male attributes has not been considered so far. Similarly, the fact that males with large antlers father more calves (Kruuk et al. 2002
) has been interpreted as being the result of these males winning more fights and forming larger harems, excluding the possibility that males may also signal their fertility or their competitive ability after copulation, and that female choice may play a role. 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. We address the question of whether this complex design and extreme size may also convey information about the reproductive potential of the male.
Our results show that relative antler size and complexity are honest indicators of sperm production and of sperm velocity in male red deer (Cervus elaphus hispanicus
), thus providing support for the phenotype-linked fertility hypothesis, which states that functional fertility covaries with male phenotype (Sheldon 1994
The two variables used in our study are known to influence male fertilization success, both in competitive and non-competitive contexts. Relative testes size determines sperm production rate (Setchell 1978
; Møller 1989
; Gomendio et al. 1998
) and thus indicates the number of sperm present in each ejaculate, the number of ejaculates that can be produced in time, and the ability to avoid sperm depletion (Wedell et al. 2002
). The number of sperm in each ejaculate determines fertilization success mainly because large numbers of sperm are needed to avoid the dilution effects and the high mortality rates that sperm suffer within the female reproductive tract (Short 1981
). The importance of sperm numbers is exacerbated when ejaculates from rival males compete, resulting in a greater investment in testes size when there is sperm competition. The benefits derived by males from producing more sperm when they face competition with other males must be almost universal, since in most taxa, species with high levels of sperm competition have larger testes: butterflies (Gage 1994
); fishes (Stockley et al. 1997
); birds (Møller 1991
; Birkhead 1996
); frogs (Jennions & Passmore 1993
); primates (Short 1979
; Harcourt et al. 1981
); mammals (Kenagy & Trombulak 1986
); ungulates (Ginsberg & Rubenstein 1990
); for a review see Parker et al. (1997)
. Using an experimental approach, it has been demonstrated that sperm competition does select for an increase in testes size (Hosken & Ward 2001
More recent evidence has shown that, in addition to numbers, sperm quality also influences male fertilization success. Sperm velocity seems to play an important role, both in competitive and non-competitive contexts (Birkhead et al. 1995
; Holt et al. 1997
; Froman et al. 2002
; Moore et al. 2002
; Gage et al. 2004
). Sperm velocity and vigour may determine sperm ability to overcome physical barriers in the female tract, to enter or leave sperm storage tubules, and to penetrate ova vestments (Froman et al. 1999
). In addition, when sperm from rival males compete, sperm velocity may determine which sperm arrive first to the vicinity of the ova, and are thus more likely to fertilize.
To obtain an overall measure of sperm velocity, we performed a multivariate analysis including six sperm motility objective parameters. This analysis generated a reliable index of sperm velocity: first, all the variables contribute significantly to the sperm velocity component obtained; second, the variance accounted for by this component was 50%; third, all the variables behaved according to the predictions.
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. The results of the multivariate analysis show that all the measures correlate highly significantly with the relative antler size component extracted, and that the variance accounted for by this component is 62%. Since all our antler measurements were corrected for body length, our overall indicator of antler size is not confounded by individual differences in body size.
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. Since it is known that environmental variables, such as population density, and their effects upon physical condition may influence antler size (Andersson 1994
; Kruuk et al. 2002
), we included kidney fat index and population in our analyses to test whether they could be influencing the relationship between antler size/complexity and sperm production/quality. However, our analyses show that both variables had no significant effect in our models, suggesting that the relationship between antlers and sperm production and quality is not confounded by these effects. In addition, male age and time of culling had no effect on relative testes size and sperm velocity, thus eliminating the possibility that they may have explained in part the relationship found.
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 three possible benefits for the female that could explain the function of antlers as honest indicators of male reproductive quality. One of the possible benefits is infertility avoidance. Although it has been argued that this kind of benefit is unlikely because male infertility would be strongly selected against in natural populations (Birkhead 1996
), at this stage we cannot rule out the possibility that the differences observed between males in ejaculate quality (e.g. Roldan et al. 1998
) may translate into differences between males in fertility rates large enough to influence female choice. The evidence showing that both sperm production and sperm swimming velocity influence fertilization success (Holt et al. 1997
; Gomendio et al. 1998
; Levitan 2000
) lends support to the possibility that antlers may be signalling precisely those reproductive traits that determine male fertility. Second, 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 (Wedell et al. 2002
). Red deer are seasonal breeders and the rut begins at the end of the summer and lasts for two to three months. During the rut, males may defend harems or territories and copulate frequently with several females (Clutton-Brock et al. 1982
; Carranza et al. 1990
). Thus, it is possible that male deer will become sperm-limited as the rut progresses, as has been previously shown in another seasonal ungulate (Preston et al. 2001
). However, sperm depletion is mainly the result of a reduction in the number of sperm available. The fact that antler size and complexity are associated with sperm velocity suggests that signalling sperm depletion may not be the main function of antlers.
A third possibility is that male antlers advertise ejaculate competitiveness, which determines fertilization success under sperm competition, although the prevalence of sperm competition in red deer populations is currently believed to be limited. In red deer populations from northern Europe, males tend to defend harems but females may copulate with several males during a given sexual cycle since they change harems. This possibility is supported by the fact that in our model species (Cervus elaphus
) males have large testes in relation to their body size when compared with other species from the Cervidae
family (Clutton-Brock et al. 1982
). Moreover, in populations from southern Europe such as those included in this study, the mating season coincides with a period of food scarcity, since it begins after the hot and dry summer and takes place largely before the rains start. 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
). 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
). Thus, in this context, sperm competition may be more intense, and females more able to choose which males they copulate with.
These three alternatives suggest that by choosing to copulate with males with large and complex antlers females could increase the chances of mating with fertile males; with males which are unlikely to become sperm depleted soon after the reproductive season begins, and/or with males which are likely to win in a sperm competition context. There are some suggestions in literature supporting the existence of female choice in red deer (Lincoln & Guinness 1973
; Bartos 1982
; Bubenik 1983
), and it has been shown that female red deer choose males because 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. Both antler size (Williams et al. 1994
; Kruuk et al. 2002
) and semen quality are, to a certain extent, heritable (Beatty 1971
; Ansah et al. 1985
; Humblot & Ducrocq 1996
; Froman et al. 2002
; Simmons & Kotiaho 2002
), 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 fertilizations both in competitive and non-competitive contexts and the possible preferences shown by females to mate with them.