Sperm competition occurs when a female copulates with two or more males and the sperm of those males compete within the female's reproductive tract to fertilize her eggs. The frequent occurrence of sperm competition has forced males of many species to develop different strategies to overcome the sperm of competing males. A prevalent strategy is for males to increase their sperm investment (total number of sperm allocated by a male to a particular female) after detecting a risk of sperm competition. It has been shown that the proportion of sperm that one male contributes to the sperm pool of a female is correlated with the proportion of offspring sired by that male. Therefore, by increasing his sperm investment a male may bias a potential sperm competition in his favour. Here we show that male meadow voles, Microtus pennsylvanicus, increase their sperm investment when they mate in the presence of another male's odours. Such an increase in sperm investment does not occur by augmenting the frequency of ejaculations, but by increasing the amount of sperm in a similar number of ejaculations.
Olfactory communication in primates is gaining recognition; however, studies on the production and perception of primate scent signals are still scant. In general, there are five tasks to be accomplished when deciphering the chemical signals contained in excretions and secretions: (1) obtaining the appropriate samples; (2) extracting the target organic compounds from the biological matrix; (3) separating the extracted compounds from one another (by gas chromatography, GC or liquid chromatography, LC); (4) identifying the compounds (by mass spectrometry, MS and associated procedures); and (5) revealing biologically meaningful patterns in the data. Ultimately, because some of the compounds identified in odorants may not be relevant, associated steps in understanding signal function involve verifying the perception or biological activity of putative semiochemicals via (6) behavioral bioassays or (7) receptor response studies. This review will focus on the chemical analyses and behavioral bioassays of volatile, primate scent signals. Throughout, we highlight the potential pitfalls of working with highly complex, chemical matrices and suggest ways for minimizing problems. A recurring theme in this review is that multiple approaches and instrumentation are required to characterize the full range of information contained in the complex mixtures that typify primate or, indeed, many vertebrate olfactory cues. Only by integrating studies of signal production with those verifying signal perception will we better understand the function of olfactory communication.
Signal complexity has been linked to social complexity in vocal, but not chemical, communication. To address this gap, we examined the chemical complexity of male and female glandular secretions in eight species of Eulemur. In this diverse clade of macrosmatic primates, species differ by social or mating system and dominance structure. We applied principal component and linear discriminate analyses to data obtained by gas chromatography/mass spectrometry. Beyond the significant effects on chemical signals of gland type, sex, season and species, we found effects of social variables and phylogeny. Notably, female odours were more chemically complex in multimale-multifemale species than pair-bonded species, whereas male odours were more chemically complex in codominant species than female-dominant species. Also, the traditional sexual dimorphism, whereby male signal complexity exceeds that of females, was present in codominant species, but reversed in female-dominant species. Lastly, a positive relationship between the species' pairwise chemical distances and their pairwise phylogenetic distances supported a gradual, but relatively fast mode of signal evolution. We suggest that the comparative method can be a powerful tool in olfactory research, revealing species differences relevant to the understanding of current signal utility and evolutionary processes. In particular, social complexity in lemurs may have selected for olfactory complexity.
Studies of chemical signals in vertebrates typically target single species; however, a broader understanding of olfactory communication may derive from comparative studies. We collected urine from 12 species representing most families of strepsirrhine primates – an excellent model clade because of variation in scent marking and socioecology. Using SPDE/GC–MS, we identified the volatile chemical composition of male and female urine from six ‘urine marking’ species and six glandular or ‘non‐urine marking’ species. We found no sex differences, but as predicted, urine markers expressed the most chemically complex and distinctive urine. More distantly related species had more dissimilar urinary profiles, suggesting gradual signal evolution. Reconstructing ancestral chemical profiles revealed different evolutionary trajectories for urine and non‐urine markers. We suggest that urine marking is an ancestral behaviour related to solitary, nocturnal living and that parallel evolutionary shifts towards greater reliance on derived glandular marking occurred in a family (Lemuridae) characterized by diurnality and sociality.
Some non-human animals may possess the ability to recall the "what", "where", and "when" of a single past event. We tested the hypothesis that male meadow voles possess the capacity to recall the "what", "where", and "when" of a single past event associated with mate selection in two experiments. Briefly, male voles were allowed to explore an apparatus that contained two chambers. One chamber contained a day-20 pregnant female (24 h prepartum). The other chamber contained a sexually mature female that was neither pregnant nor lactating (REF female). Twenty-four hour after the exposure, the males were placed in the same apparatus, which was empty and clean. At this time, the pregnant female would have entered postpartum estrus (PPE), a period of heightened sexual receptivity. Males initially chose and spent significantly more time investigating the chamber that originally housed the pregnant female (now a PPE female) than the chamber that originally housed the REF female. Male voles also explored an apparatus containing a chamber with a PPE female and one chamber containing a REF female. Twenty-four hour later, males were placed into an empty and clean apparatus. The males did not display an initial choice and they spent similar amounts of time investigating the chamber that originally housed the PPE female (now a lactating female) and the chamber that originally housed the REF female. The results of these and additional experiments suggest that male voles may have the capacity to recall the "what", "where", and "when" of a single past event, which may allow males to remember the location of females who would currently be in heightened states of sexual receptivity.
Is it possible that voles have a sense of number? To address this question, we determined whether voles discriminate between two different scent-marking individuals and identify the individual whose scent marks was on top more often than the other individual. We tested whether voles show a preference for the individual whose scent marks was on top most often. If so, the simplest explanation was that voles can make a relative size judgement-such as distinguishing an area containing more of one individual's over-marks as compared to less of another individual's over-marks. We found that voles respond preferentially to the donor that provided a greater number of over-marks as compared to the donor that provided a lesser number of over-marks. Thus, we concluded that voles might display the capacity for relative numerousness. Interestingly, female voles were better able than male voles to distinguish between small differences in the relative number of over-marks by the two scent donors.
Sperm competition theory predicts that under high risk of sperm competition, males will increase the number of sperm that they allocate to a female. This prediction has been supported by some experimental studies but not by others. Here, I conducted a meta‐analysis to determine whether the increase in sperm allocation under high risk of sperm competition is a generalized response across taxa. I collected data from 39 studies and 37 species. Across taxa, males under a high risk of sperm competition respond by increasing their sperm allocation (mean effect size = 0.32). Number of offspring did not explain a significant portion of the variation in effect sizes. A traditional meta‐analysis (i.e. without phylogenetic information) described the variation among effect sizes better than a meta‐analysis that incorporates the phylogenetic relationships among species, suggesting that the increase in sperm allocation under high risk of sperm competition is similarly prevalent across taxa.
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