Is baculum length influenced by sexual selection?

The sexual selection was defined by Darwin in 1871 as the advantage which certain individuals have over other individuals of the same sex and species, in exclusive relation to reproduction. It can be divide in two components. The first one is the pre-copulatory selection, which happens before the copulation via male competition, and via classic female choice for a mate. The one we are interested in is the postcopulatory selection, which cover all the events during and after the copulation. We can make an analogy with the precopulatory selection : the male-male battle of the pre-copulatory selection is equivalent to the sperm competition, and the classic female choice is similar to the cryptic female choice for the spermatozoa. The sperm competition occurs when the sperm from two or more males compete to fertilize a set of ova (Parker 1970; Birkhead & Møller, 1998).

The postcopulatory sexual selection is known to be a strong selective force driving the evolution of behavioral and morphological sexual traits (Andersson 1994).

The genitalia structure studied here is the baculum, the penis bone present in some species of mammals within the following orders : Chiroptera, Rodentia, Carnivora, Primates. The development of the baculum is highly variable among species, a characteristic which allows us to think that post-copulatory selection could be a factor that influence its morphology. Indeed, even closely related species show a great diversity of the baculum length and shape. Here, we are going to focus on baculum length.

Because of this diversity, the baculum function remains uncertain. Four main hypotheses are actually proposed : prolonged intromission, induced ovulation, vaginal friction, and indicator of genetic quality in males (Lariviere and Ferguson 2002).

The first hypothesis suggests that the baculum assists in sperm transport. This can lead to an increase of the baculum length in species which prolong intromission into the post-ejaculatory period (Dixson 1987) and in species that have a single prolonged intromission instead of several short ones. The distal head could also contribute to displacing or damaging sperm from previous males (Fairbairn et al. 2003).

According to the second one, the additional rigidity provides by the baculum could also be a way to stimulate the reproductive tract of the female to induce ovulation, and so increasing the likelihood of successful fertilization. The vaginal friction hypothesis could happen when the sexual dimorphism is strong, the baculum could help to support the increasing friction due to a relative small vagina opening by providing additional rigidity. Therefore, these hypotheses - except the last one - are not supported by everybody, but no better explanations can actually be found.

The aim of the study is to determine whether the baculum length of mammal is influenced by the post-copulatory sexual selection. To assess this relation, we need to evaluate the sexual selection intensity.

The type of mating system influence the intensity of the post-copulatory sexual selection. Indeed, in a polygamic system, where more than one male tends to mate with each fertile female, the sperm competition will be higher than in monogamic system. Then, if the sperm competition is high, because sperm is produced in the testes, the testes should be relatively large. Indeed, larger testes produce higher quality ejaculates (number of sperm, ejaculate volume and motility) and have higher rates of sperm production. Thus, males with larger testes are assumed to have higher reproductive success than males with small testes in species with sperm competition.

Because of the strong correlation between intensity of the post-copulatory sexual selection and the relative testes mass (Harcourt et al. 1981), we can use relative testis mass as a proxy measure of postcopulatory sexual competition.

For this study, the data were taken from already published data. Thus, the data set shows some biases. Indeed testes can differ in size between individuals, and vary across seasons : species with breeding seasons have unusually large testes. So it depends of the season measurement and if testes and body mass were taken on the same individual. However, the interspecific differences are supposed to be important enough so they are not influenced by intraspecific effects such as mass differences between individuals.

Body weight and testes weight were logarithmicaIly transformed before statistical analysis in order to normalize the data as far as possible and hence equalize variances. One regression was done for each order (Primates, Carnivora, Rodentia, Chiroptera), and one another inter-order, to give a general idea.The first step is to calculate the linear regression of testes mass against body mass, and use the residuals from this regression as an indicator of the selection intensity (relative testes mass). Using residuals allows easy comparison of testes weights, with the effect of body weight removed.

Figure 1 : Plot of the regression testes mass against body mass

Then, the linear regression baculum length against body mass was calculated, in order to use the residuals (relative baculum length).

Figure 2 : Plot of the regression baculum length against body mass

The last regression was testes residuals against baculum residuals. This regression is the one required to answer the question : does the postcopulatory sexual selection influence the baculum length?

Either a negative or a positive allometry (where trait size increases slower for negative and faster for positive than does body size) can be expected for the regression relative testes mass against relative baculum length. Indeed, a negative allometry is usually detected on analysis of genital mass relative to body mass, but the general pattern for sexually selected trait is a positive allometry (Lupold et al. 2004). One of the explanation for this pattern is that unless there is size assortative mating, males are selected to fit average-sized females (Eberhard et al. 1998). This results in stabilizing selection, so low variability in genital size within species, and hence negative genital allometry (Hosken and Stockley 2004).

Figure 3 : Plot of the regression relative baculum length against relative testes mass

The results of this study do not show a correlation between baculum length and relative testes mass, except for the primates. But I wasn't using any phylogenetic control, which can create an important bias. Indeed, in a similar study on Chiroptera, after controlling for phylogeny, no significant associations were found in their data set. This suggests that the species-level result was due to phylogenetic non-independence. and that the baculum is not influence by the intensity of postcopulatory sexual selection.

Moreover, the high diversity of the baculum among the species might be so great that we cannot show any pattern by working at the order level. This can be the case if the baculum plays a different role in every taxon, which can also explain difficulties to find out the baculum function.

But fore some researchers working on this subject, a lack of correlation between baculum length and relative testes mass cannot lead us to conclude that postcopulatory sexual selection doesn't influence genital length. Such a finding could equally result from the action of other forms of sexual selection (Hosken and Stockley 2004). Indeed, four main sexual selection mechanisms are implicated in genital evolution sexy sons, good genes (both part of the cryptic female choice), sexual conflict and of course sperm competition.

Sexual conflict is driven by the opposed reproductive interests in females and males that result in sexually antagonistic behavior and coevolving adaptations. Good-genes sexual selection models predict that females will preferentially fertilize their ova with the sperm of high quality males in order to gain genetic benefits for their offspring (reviewed in Andersson 1994). According to the sexy son hypothesis, females are assumed to compensate for their direct inferior breeding success by the increased number of descendents produced by their sexy sons. The main difference between good genes and sexy sons is that sexy sons hypothesis assumes an indirect effect due to the attractiveness of the sons whereas good genes focus on viability in sons and daughters (Huk and Winkel 2008).

As a conclusion, even if we did not show a correlation between baculum length and the intensity of the postcopulatory sexual selection, some other components of the sexual selection could influence the evolution of genital length. Some more studies are necessary to discover what is really the function of the baculum, and what influence its great diversity.

Citations

Birkhead TR, M0ller AP (1998) Sperm competition and sexual selection. Academic Press, London

Dixson AF (1987) Observations on the evolution of the genitalia and copulatory behaviour in male primates. J Zool (Lond) 213:423-443

Eberhard WG, Huber BA, Rodriguez RL, Briceno SRD, Salas I, Rodriguez V (1998) One size fits all? Relationships between the size and degree of variation in genitalia and other body parts in twenty species of insects and spiders. Evolution 52:415-431

Harcourt AH, Harvey PH, Larson SG, Short RV (1981) Testis weight, body weight and breeding system in primates. Nature 293:55-57

Lüpold, S., Mcelligott, a G. & Hosken, D.J., 2004. Bat genitalia: allometry, variation and good genes. Biological Journal of the Linnean Society, 83(4), pp.497-507.

Lariviere, S. & Ferguson, S.H., 2002. On the evolution of the mammalian baculum: vaginal friction, prolonged intromission or induced ovulation? Mammal Review, 32(4), pp.283-294.

Huk, T. & Winkel, W., 2007. Testing the sexy son hypothesis--a research framework for empirical approaches. Behavioral Ecology, 19(2), pp.456-461.

Hosken, D.J. & Stockley, P., 2004. Sexual selection and genital evolution. Trends in ecology & evolution (Personal edition), 19(2), pp.87-93.