Scent and the single male: ring-tailed lemurs produce honest signals


  • doi: 10.1111/j.1365-294X.2008.03834.x

Cheryl S. Asa, Fax: 314-646-5534; E-mail:


In mating systems that involve competing males and choosy females, males are expected to advertise their genetic quality to discriminating females. Most examples have focused on visual or acoustic signals, such as ornamentation or song; yet arguably, olfactory communication may be more important to the majority of vertebrates with the possible exception of birds. Fortunately, attention has begun to shift to the role of odours in mate choice, with most of that attention being directed at the major histocompatibility complex or more recently at the major urinary proteins. The study of male ring-tailed lemurs presented by Charpentier and colleagues in this issue adds a new dimension to investigations of the influence of genes on mate choice via odour production. By comparing genetic heterozygosity to the production of semiochemicals in the scrotal scent gland, they provide a link between genetic composition and scent-marking behaviour as a potential advertisement of male quality.

Olfactory communication was a popular area of study in the 1970s and 1980s fuelled by advances in neurophysiology and the enlistment of analytical techniques for identifying odorants (Doty 1976; Muller-Schwarze & Silverstein 1980; Albone 1984; Muller-Schwarze 2006). Detailed descriptions of the vomeronasal organ (VNO) and the neuroanatomy of the main and accessory olfactory tracts stimulated interest in their function (Scalia & Winans 1975; Wysocki 1979). Gas chromatography and mass spectrometry revealed many of the volatile compounds, semiochemicals, that composed various types of scent marks in many species (Novotny et al. 1974a,b; Albone 1984). Currently, because of advances in molecular genetics, interest in the study of scent has been reinvigorated, in particular, in the relationship of genes and scent production. Evidence is accumulating that genetic identity can be represented by what amounts to an odour fingerprint. The hypervariable major histocompatibility complex (MHC) and, more recently, the major urinary proteins (MUP) have emerged as likely candidates, producing odorants that can serve to identify individuals (Cheetham et al. 2007; Sherborne et al. 2007).

The study by Charpentier et al. (2008) in this issue investigates two other aspects of genetic identity reflected in male scent glands: (i) population heterozygosity (degree of inbreeding) and (ii) relatedness among the population's males (relative genetic distance). The study is especially interesting because it focuses on a primate that has a rich repertoire of scent-marking glands and behaviours (ring-tailed lemur, Lemur catta, Fig. 1). The authors found that the complexity of scrotal scent samples (e.g. the diversity of compounds identified per sample) was related both to heterozygosity and to the genetic distance between males, two factors believed to be involved in mate choice. A female would be expected to generally favour outbred to inbred males and also to assess her genetic distance from prospective partners to maximize fertility.

Figure 1.

Male ring-tailed lemurs scent mark with scrotal secretions that advertise their genetic heterozygosity and relative genetic distance from each other. The information in these secretions may also be used by females to judge the genetic quality of potential mates. (Photo credit: Chuck Dresner, courtesy of the Saint Louis Zoo)

Most studies of the role of olfaction in mate choice have used urine and related it to variability at the MHC or MUP, but they have not analyzed the actual components of the urine samples (see Cheetham et al. 2007; Sherborne et al. 2007). Variability of urine constituents by individual animal has been assumed but not documented. In this study by Charpentier and colleagues, the actual components have not been presented, but the elution profiles show clear differences between homozygous and heterozygous males.

The elution profiles also revealed the surprising result that scent complexity was greater during the nonbreeding season than during the breeding season. As would be predicted, scent-marking behaviour was higher during the breeding season, so the reduction in complexity of scent marks during that time seems paradoxical. In general, testosterone has been shown to stimulate both the production of glandular secretions used in scent marking and the scent-marking behaviour itself (Strauss et al. 1970; Asa et al. 1990). Thus, it would be reasonable to expect additional components, not fewer, during the breeding season when androgens are elevated. However, androgens do not always cause production of more scent components. In our work with volatile chemicals in the urine of wolves, we found that treating castrated males with testosterone induced production of some compounds typically found in intact males while reducing levels of some compounds found in castrates and females (Raymer et al. 1986). Those results indicate that, at least in urine, testosterone can inhibit some components although it stimulates others.

The authors present an interesting possible explanation for the number of scrotal scent constituents being lower in ring-tailed lemurs during the breeding season. Because glucocorticoids are also elevated at that time, attributed to the increase in aggressive interactions likely stimulated by androgens, they hypothesize that the glucocorticoids may have had negative effects on scent constituent production. Neither glucocorticoid nor androgen concentrations were reported for this study; therefore, it would be interesting to directly compare those levels with scent component complexity. In at least one other primate, scent marks from one male can suppress plasma testosterone in another male (Perret & Schilling 1987); thus, it cannot be assumed that all males had equivalent levels of testosterone.

Another possible interpretation involves the chemical components that are missing during the breeding season. They appear to be primarily those of higher volatility or lower molecular weight, judging by their shorter retention times. There are at least two possible explanations for this pattern. First, compounds of higher volatility can be produced by microbial action that breaks down compounds into smaller components that are of lower molecular weight and thus more volatile (Albone 1984). Is it possible that the larger molecular weight constituents are being produced at a higher rate during the breeding season? Because the scent-marking frequency is also higher, so that the contents are being emptied more regularly, there might be less time for microbial action to produce the lower molecular weight compounds.

Secondly, the pheromones most often implicated in courtship and mating are of higher molecular weight and lower volatility, since they are used primarily when animals are in close proximity or are directly in contact. Thus, the higher volatility components may be less relevant during the breeding season. Furthermore, the presence of a component does not necessarily mean that it contains an important olfactory meaning, nor does the amount of a component reflect a proportional importance.

There are many interesting directions the authors could take to follow on the results of this study. One, of course, is to evaluate the responses of females to the scrotal scents, to determine whether they do indeed make the predicted choices that result in the best genetic fit for them. It would also be interesting to know whether the scrotal scents advertise ‘good genes’, that is, specific alleles that increase fitness. Heterozygosity as an indicator of the degree of inbreeding can represent genetic quality and may be especially important in small populations, in which inbreeding can be a greater threat. The implications for small or fragmented populations of endangered species could be dire if females detect and refuse to mate with closely related males.