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Sexual Signalling in Propithecus verreauxi: Male “Chest Badge” and Female Mate Choice

  • Stefania Dall'Olio,

    Affiliations Centro Interdipartimentale Museo di Storia Naturale e del Territorio, Università di Pisa, Pisa, Italia, Dipartimento di Biologia Evoluzionistica, Università di Firenze, Firenze, Italia

  • Ivan Norscia,

    Affiliation Centro Interdipartimentale Museo di Storia Naturale e del Territorio, Università di Pisa, Pisa, Italia

  • Daniela Antonacci,

    Affiliation Centro Interdipartimentale Museo di Storia Naturale e del Territorio, Università di Pisa, Pisa, Italia

  • Elisabetta Palagi

    betta.palagi@museo.unipi.it

    Affiliations Centro Interdipartimentale Museo di Storia Naturale e del Territorio, Università di Pisa, Pisa, Italia, Istituto di Scienze e Tecnologie della Cognizione , Consiglio Nazionale Delle Ricerche, Roma, Italia

Sexual Signalling in Propithecus verreauxi: Male “Chest Badge” and Female Mate Choice

  • Stefania Dall'Olio, 
  • Ivan Norscia, 
  • Daniela Antonacci, 
  • Elisabetta Palagi
PLOS
x

Abstract

Communication, an essential prerequisite for sociality, involves the transmission of signals. A signal can be defined as any action or trait produced by one animal, the sender, that produces a change in the behaviour of another animal, the receiver. Secondary sexual signals are often used for mate choice because they may inform on a potential partner's quality. Verreaux's sifaka (Propithecus verreauxi) is characterized by the presence of two different morphs of males (bimorphism), which can show either a stained or clean chest. The chest becomes stained by secretions of the sternal gland during throat marking (rubbing throat and chest on a vertical substrate while smearing the scent deposition). The role of the chest staining in guiding female mate choice was previously hypothesized but never demonstrated probably due to the difficulty of observing sifaka copulations in the wild. Here we report that stained-chested males had a higher throat marking activity than clean-chested males during the mating season, but not during the birth season. We found that females copulated more frequently with stained-chested males than the clean-chested males. Finally, in agreement with the biological market theory, we found that clean-chested males, with a lower scent-releasing potential, offered more grooming to females. This “grooming for sex” tactic was not completely unsuccessful; in fact, half of the clean-chested males copulated with females, even though at low frequency. In conclusion, the chest stain, possibly correlated with different cues targeted by females, could be one of the parameters which help females in selecting mates.

Introduction

Communication, an essential prerequisite for sociality, involves the transmission of signals [1], [2]. A signal can be defined as any action or trait produced by one animal, the sender, that produces a change in the behaviour of another animal, the receiver [3]. The transfer of messages, either born or not by signals [4], can be beneficial to either senders, receivers, or both [5]. Secondary sexual signals (visual, acoustic or chemical) are often used for mate choice because they may inform on a potential partner's quality [6]. In bipedal vertebrates, mate choice often relies on visual sexual signals that are placed frontally to the observer. This situation occurs quite frequently in birds. Peacock (Pavo cristatus) tail spreading [7], the level of symmetry in chest plumage of male zebra finches (Taeniopygia guttata) [8], and the size of the black feather bib on the throat of male house sparrows (Passer domesticus) [9] are just three examples of secondary visual sexual signals used by females to choose mating partners. Within the primate order, some observers have reported that also in humans (Homo sapiens), women's sexual selection appears to be influenced by the amount of chest hairs in males [10]. Men's choice can be affected by size and symmetry of women's breasts [11][13], a signal that in humans is exaggerated compared to other primates [14], [15]. Quadruped locomotion habits and chest sexual signals do not generally co-exist due to obvious perceptual constraints.

Frontal visual signals can be favoured by sexual selection when three conditions are met: 1) a diurnal lifestyle, which makes visual signals detectable; 2) upright locomotion, which makes face and/or chest signals visible; 3) a mating system based on either female or male mate choice and strong intra-sexual competition [16].

In primates, besides humans, only a few species meet such conditions [17]. Orang-utans are one of the most sexually dimorphic apes with dimorphism in size, adornments, and vocal signals [17]. Orang-utans are characterized by an irreversible bimorphism and fully mature males can show frontal sexual adornments, which consist of cheek flanges and a throat pouch, a sort of chest “badge” [18]. Males without such secondary sexual features are generally named as “unflanged” males which, under particular social circumstances (e.g. the absence of a flanged male), can acquire in a few months the adornments typical of flanged males [19].

Verreaux's sifaka (Propithecus verreauxi) is a diurnal prosimian species characterized by upright locomotion (bipedal hopping and leaping; [20]) and male intra-sexual competition [21]. There is a lack of sexual dimorphism in body size and females are dominant over males [20], [22]. These characteristics make it impossible for males to coerce female copulation and promotes female mate choice [20], [22][24]. Lewis [25] reported bimorphism in male sifakas, which can show either a stained or unmarked chest, as a function of scent-marking activity during which the throat and chest are rubbed up against a substrate, often multiple times within a single marking bout [26]; Table 1. (Fig. 1). In prosimians, glandular scent-marking has a variety of social functions such as advertisement and territorial defense (Propithecus verreauxi, [25]; Propithecus edwardsi, [27]; Lemur catta [28]), intergroup communication (Propithecus verreauxi [25]), advertisement of social dominance (Lemur catta, [29]), signaling of reproductive condition (Lemur catta, [30], [31]), and mate selection (Nycticebus pygmaeus [32]; Propithecus verreauxi, [22]). About half of the scent marks by sifaka males are overmarks, in which a scent mark is placed on or near a female scent mark [25] and thus, in cases of intense activity, the staining of the chest is probably a combination of a male's own glandular secretions, female anogenital secretions, female urine, and dirt [26]. Lewis and van Schaik [26] described this male phenotypic variation (stained versus clean-chested males) as a form of reversible bimorphism. However, the authors did not find any clear evidence that the two morphs of males differ in their intrinsic physical characteristics, such as body size and maxillary canine length [26]. Norscia et al. [22] demonstrated that females gave copulatory priority to males who more frequently countermarked female scent depositions. However, results demonstrating a clear link between male chest bimorphism and female mate choice are still lacking.

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Figure 1. The two different morphs of sifaka males.

An example of stained-chested male (on the left, photo by E. Palagi). The brown smear, particularly evident on the throat, extends to the upper part of the chest (dark/brown, photo by I. Norscia). An example of clean-chested male (on the right). No brown smear is present on the throat.

https://doi.org/10.1371/journal.pone.0037332.g001

Here, we decided to test whether or not sifaka females' mating patterns are associated with the male chest badge, which seems to correlate with male scent-marking and dominance [25], [26]. We made the following predictions:

Prediction 1

Lewis's findings [25] suggest that while clean-chested males deposit scents for inter-group communication, stained-chested males release scent depositions for mate-guarding purposes. Moreover, during the birth season, testes mass (and, possibly, in testosterone levels) do not differ between clean- and stained-chested males [33]. If the stained chest is a signal linked to male intra-sexual competition (ultimate cause) and to testosterone levels (proximate cause), we expect stained-chested males to show a higher throat-marking frequency than the clean-chested males during the mating season but not necessarily during the birth season.

Prediction 2

Lewis and van Schaik [26] reported that stained-chested males are generally dominant in their social groups. Thus, if a stained chest is one of the possible signals which females can use in their mate choice, we predict stained-chested males will copulate more frequently than the clean-chested males.

Prediction 3

In the mating market, the balance of power tilts in favor of females whenever males cannot force them into mating [24], especially when females are dominant. Consequently, males depend on females for breeding opportunities and must compete to prove their superiority to females, thus increasing their possibility to be selected [24], [34]. Males can engage in both contest competition via physical/ritualized fighting and outbidding competition, in which a male plays off rivals by making a better offer [35]. In the latter case, males can secure the favors of a female by advertising their quality (e.g. the dominance status) through visual or olfactory displays [36], [37] and/or by providing commodities in exchange for female access [38], [39]. In sifaka, the mating system follows the biological market rules where both scent-marking and grooming are good male services on which females base their mate selection [22]. Norscia et al. [22] found that to obtain priority and/or a high number of copulations sifaka males had to be top-scent releasers and/or females' top-groomers. According to the biological market theory, we expect that clean-chested males, with lower scent-releasing potential [26], in order to have some copulation opportunities need to compensate by offering more grooming to females than stained-chested males.

Results

Prediction 1 supported

During the mating season stained-chested males (mean ±SE: 2.07±1.15 times per hour) throat marked significantly more often than clean-chested males (mean ±SE: 0.19±0.11 times per hour) (two independent samples randomization test: t = −1.789; nc = 6, ns = 5, p = 0.018; Fig. 2). A significant difference was also found in the use of genital glands by the two morphs of males (stained-chested males, mean ±SE: 0.29±0.17 times per hour; clean-chested ones, mean ±SE: 0.02±0.01 times per hour; two independent samples randomization test: t = −1.688, nc = 6, ns = 5, p = 0.045).

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Figure 2. Marking activity in the mating season.

Frequency of throat marking performed by clean- and stained-chested males during the mating season. Solid horizontal lines indicate medians; length of the boxes corresponds to inter-quartile range; thin horizontal lines indicate range of observed values.

https://doi.org/10.1371/journal.pone.0037332.g002

During the birth season the difference in the throat-marking between stained- and clean-chested males disappeared (stained-chested males, mean ±SE: 3.52±1.03 times per hour; clean-chested ones, mean ±SE: 0.54±0.26 times per hour; two independent samples randomization test: t = 2.801, nc = 3, ns = 3, p = 0.140); no difference was also found for genital depositions (stained-chested males, mean ±SE: 1.49±0.19 times per hour; clean-chested ones, mean ±SE: 0.07±0.18 times per hour; two independent samples randomization test: t = 7.151, nc = 3, ns = 3, p = 0.105). The seasonal difference in the sample size (11 males, mating season; 6 males, birth season) is due to the presence of out-group males in our study groups during the mating period [40].

Prediction 2 supported

In the mating season, the stained-chested males engaged in significantly more copulation events per hour (mean ±SE: 0.59±0.12) than the clean-chested ones (mean ±SE: 0.12±0.06) (two independent samples randomization test: t = −3.587, nc = 6, ns = 5, p = 0.0016; Fig. 3).

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Figure 3. Copulation events of the two different morphs of males.

Frequency of copulation events performed by clean- and stained-chested males. Solid horizontal lines indicate medians; length of the boxes corresponds to inter-quartile range; thin horizontal lines indicate range of observed values.

https://doi.org/10.1371/journal.pone.0037332.g003

Prediction 3 supported

In the mating season females received more grooming from clean-chested males (mean ±SE: 0.06±0.02 times per minute) than from stained-chested ones (mean ±SE: 0.14±0.00 times per minute) (paired samples randomization test: t = 2.035, n = 6, p = 0.028; Fig. 4a). This difference vanished in the birth season (paired samples randomization test: t = −0.81, n = 6, p = 0.499; Fig. 4b).

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Figure 4. Grooming received by females.

Frequency of grooming received by each female from clean- and stained-chested males (a) during the mating season and (b) during the birth season. Solid horizontal lines indicate medians; length of the boxes corresponds to inter-quartile range; thin horizontal lines indicate range of observed values.

https://doi.org/10.1371/journal.pone.0037332.g004

Discussion

In this paper, we found that stained-chested males had a higher throat and genital-marking activity than clean-chested males during the mating season but not during the birth season (Prediction 1 supported). Moreover, we found that females copulated more frequently with stained-chested males (including both resident and non-resident) than with clean-chested males (including both resident and non-resident) (Prediction 2 supported), even though the latter offered more grooming to females compared to the former during the mating season (Prediction 3 supported).

Males of several mammalian species modulate their scent-marking activity according to their perceived mating opportunities [41], [42] and can increase their plasma testosterone concentration, as well as scent-marking, when they are sexually stimulated [43]. In the mating season a scent-marking dichotomy between the two different morphs of sifaka males existed (stained-chested males scent-marked more frequently than clean-chested ones). This dichotomy disappeared during the birth season, when males were not sexually stimulated and males' intra-sexual competition decreased due to the lack of eggs to be fertilized. One of the proximate causes of the scent-marking dichotomy in the mating season is the difference in the concentration of testosterone levels between stained- and clean-chested males, which also differ in their testes mass [33]. The lack of difference in the testes mass of the two male morphs during the birth season led authors [33] to infer that stained- and clean-chested males do not differ in their testosterone levels. This is consistent with our data, which show no difference in the frequency of scent-marking rates between the two morphs of males in the birth season.

The stained-chest provides benefits to sifaka males by increasing their reproductive opportunities (“marking for sex” tactic). Copulations involved both in-group and out-group stained-chested males, this suggests that the chest badge can be functional to females, especially when they have to gather information on less familiar out-group males. This interpretation is supported by another recent finding obtained from Beza Mahafaly sifaka population, where it has been observed that most (29 of 52) of males sired at least one offspring outside their resident group [44].

Lewis and van Schaik [26] underlined the importance of multimodal signaling in Propithecus verreauxi, in which the additional visual cue of a chest stain enhances the information transmitted via the olfactory signal produced by the scent glands. Signals are frequently made up of multiple components that interact with each other to alter the receiver's response [4], [44][46]. Such multiple signals were defined as multimodal (composed of signals related to different sensory modalities) [47], [48]. The multimodality of sifaka communication is linked to its diurnal habits [20]. In fact, diurnal prosimians use multimodal signals in both reproductive and nonreproductive contexts [26], [49], [50]. Two different studies showed that both Propithecus edwardsi and Microcebus murinus females use multimodal estrus advertisement by associating a particular vaginal morphology with vocalizations [51], [52]. Palagi et al. [49] and Palagi and Dapporto [53] described urine-marking in Lemur catta as a multimodal signal composed by an olfactory cue (urine) and a visual cue (tail up, increasing the detection probability). Switching from unimodal (one cue) to multimodal signalling (more than one cue) may increase the probability of sifaka males to be promptly detected by females. Sifaka males adjust the intensity of their signal by varying its delivery frequency. Maintaining the visual chest badge is likely to be costly because it requires much effort in renewing scent depositions.

In many non-human primate species, grooming is a commodity which can be exchanged for itself or for breeding opportunities [54][56]. Grooming is one of the behaviors most frequently involved in the biological market system [35]. Within a mating marketplace, low quality males are expected to overcompensate for their quality by providing more grooming to oestrous females. Similarly, a male of high quality may be preferred by the females, and will pay a lower grooming price to be favored by them. This prediction has been supported by data coming from chimpanzees. In this species, low-ranking males need to provide more grooming to oestrus females than high-ranking males in order to gain access to females [56]. As in other primate species, grooming also seems to play an important role in sifaka. Norscia et al. [22] found that in the months immediately preceding the mating season, male grooming of females positively correlated with female grooming of males. In the mating period, this correlation disappeared because grooming was exchanged by males for copulations (“grooming for sex” tactic). Therefore, it is not surprising that during the mating season clean-chested males, due to their low testosterone levels and consequent low production of secretions (this paper; [33]), invest much more in the “grooming for sex” tactic with females than stained-chested males do. In contrast, the birth season was characterized by a lack of difference in the grooming received by females from the two morphs of males. The “grooming for sex” tactic adopted by clean-chested males during the mating season is not completely unsuccessful; in fact, half of the clean-chested males under study did copulate with females, even though their copulation frequency was significantly lower than that of stained-chested males (Figure 2). The observation that copulation frequency is higher in stained-chested males (usually dominant in their social group; [26]) than in clean-chested males is consistent with the paternity test results presented by Kappeler and Schäffler's [57], showing that sifaka dominant males can sire up to 90% of infants.

In conclusion, since the badge depends on testosterone, scent-marking, and dominance, it can represent an “overview” of males' physical state. To demonstrate the function of a potential communicative signal the experimental approach is generally required, unfortunately such approach is not feasible with this species.

Our findings that females copulate more with males showing chest stain suggest that this cue is used by females to choose mates. The choice pattern could also result from correlated expression of the stained chest with other cues that the females directly target. The clues conveyed by the badge may be used as an additional piece of information to assess the potential quality of stranger males, possessing cues that cannot be timely accessed by females.

The presence of the multiple mating tactics, “marking for sex” (stained-chested males) and “grooming for sex” (an alternative, but not completely functional, tactic used by clean-chested males) may be a means by which sifaka population buffers the inbreeding phenomenon in the small, isolated fragment of the Berenty forest [58].

Materials and Methods

Ethics statement

This study was approved by University of Pisa (Animal Care and Use board). Since the study was purely observational the committee waived the need for a permit. The study was conducted with no manipulation of animals. The study was carried out in the private Reserve of Berenty (South Madagascar) and De Heaulme family (the owner) permitted us to observe animals.

Study species and site

We conducted this study in the secondary forest of Ankoba, part of the 140-ha Berenty forest fragment (South Madagascar; S 24.99°; E 46.29°; for an extensive description see [59] on Propithecus verreauxi (Verreaux' sifaka). At Berenty, sifaka groups range from 1 to 10 individuals, according to a complete census conducted in November-December 2006 [60]. They inhabit riverine and dry forests of south and southwest Madagascar [61]. Females usually experience a single oestrus period (2–3 days) per year and both sexes can mate with multiple partners in their own and neighbouring groups, especially when a single group offers suboptimal mating opportunities [52]. In particular, males can start roaming and visiting other groups in search of oestrus females [21]. The short oestrus period and the fact that mating can be tightly synchronized within a population make copulations very difficult to detect and observe [23], [26]. Moreover, at Berenty, cyclones and heavy raining followed by river flooding normally prevent data collection in the period January-February, coinciding with sifaka's mating period. In 2007, for the first time it was possible to gather data on mating because of a prolonged drought involving South Madagascar. In the end, we gathered the highest sample of mating episodes (57 copulations) ever recorded in sifaka [22]. In May-July 2008, during the birth season, we gathered data on the same groups. This additional sample collection permitted us to compare data on marking behaviour and male-female grooming between the two different seasons (mating 2007-birth 2008).

Observational data and operational definitions

The study was conducted on adults of two sifaka groups in two different periods (mating season: 11 adult males, 6 adult females; birth season: 6 adult males, 6 adult females). Within the out-group males observed in the mating period, 2 were stained-chested and 3 were clean-chested. Animals were followed from dawn to dusk by focal (collection of grooming data) (mating season: 501 hours, birth season: 368 hours) and all occurrences animal sampling (collection of olfactory activity and copulation data) (mating season: 221 hours, birth season: 258 hours). During the mating season the authors and a field assistant collected data with daily observations of about 11 h/day. During the birth season, due to the reduced day length, the observations decreased to about 9 h/day. As typical of the sifaka the individuals of the group usually moved, rested, and foraged cohesively. However, the group could split during the mating days: in this case, the observers separated to follow the two different subgroups. We individually identified the animals according to their external features (scars, fur patches, fur color, [62]).

To distinguish stained- and clean-chested males we used the descriptions given by Lewis and van Schaik [26]. We photographed males' chest at a maximum distance of 2 m. Males with a brown, greasy spot on the chest were labeled as “stained”, whereas males with a white, clean chest were identified as “clean”. The animals with intermediate color were two out-group males (one per group) which spent in our study groups only few hours in a day. For this reason we decided to exclude them from the analysis.

Brockman [21], who observed sifaka mating in a different study site (Beza-Mahafaly; Southeastern Madagascar), provided the operational definitions used during this study (Table 1). We included in the analyses only proper copulations.

Statistical analyses

Due to the small sample size and deviation from normality (Kolmogorov-Smirnov<0.05) we used randomization procedures ([63], software: Resampling Procedures 1.3 by David C. Howell, freeware). Specifically, randomization tests were employed with a number of 10,000 permutations using resampling procedures. The software provides a t value in the same way as in a standard t test, but calculates a p value as the proportion of randomized datasets that yield an even more extreme outcome. The analyses were conducted at an individual level. All analyses were two-tailed, and the level of significance was set at 5%.

Acknowledgments

We thank the De Heaulme family and A. Jolly for the opportunity to do this research in Madagascar. We also thank S. Kaburu for helping with data collection, R. Stanyon for comments, and W. DarPrete for enlightening discussion.

Author Contributions

Conceived and designed the experiments: IN EP. Performed the experiments: SD IN DA EP. Analyzed the data: SD IN DA EP. Contributed reagents/materials/analysis tools: EP. Wrote the paper: SD IN EP.

References

  1. 1. Wilson EO (1975) Sociobiology: the new synthesis. Cambridge: Belknap University Press. 720 p.EO Wilson1975Sociobiology: the new synthesisCambridgeBelknap University Press720
  2. 2. Endler JA (1993) Some general comments on the evolution and design of animal communication systems. Phil Trans R Soc, London B 340: 215–225.JA Endler1993Some general comments on the evolution and design of animal communication systems.Phil Trans R Soc, London B340215225
  3. 3. Seyfarth RM, Cheney DL, Bergman T, Fischer J, Zuberbühler K, Hammerschmidt K (2010) The central importance of information in studies of animal communication. Anim Behav 80: 3–8.RM SeyfarthDL CheneyT. BergmanJ. FischerK. ZuberbühlerK. Hammerschmidt2010The central importance of information in studies of animal communication.Anim Behav8038
  4. 4. Rendall D, Owren MJ, Ryan MJ (2009) What do animal signals mean? Anim Behav 78: 233–240.D. RendallMJ OwrenMJ Ryan2009What do animal signals mean?Anim Behav78233240
  5. 5. Hebets A, Papaj DR (2005) Complex signal function: developing a framework of testable hypotheses. Behav Ecol Sociobiol 57: 197–214.A. HebetsDR Papaj2005Complex signal function: developing a framework of testable hypotheses.Behav Ecol Sociobiol57197214
  6. 6. Andersson M (1994) Sexual selection. Princeton: Princeton University Press. 624 p.M. Andersson1994Sexual selectionPrincetonPrinceton University Press624
  7. 7. Zahavi A (2007) Sexual selection, signal selection and the handicap principle. In: Jamieson BGM, editor. Reproductive biology and phylogeny of birds. New Hampshire: Science Publishers Enfield. A. Zahavi2007Sexual selection, signal selection and the handicap principle.BGM JamiesonReproductive biology and phylogeny of birdsNew HampshireScience Publishers Enfield
  8. 8. Swaddle JP, Cuthill IC (1994) Female zebra finches prefer males with symmetric chest plumage. Proc R Soc B 258: 267–271.JP SwaddleIC Cuthill1994Female zebra finches prefer males with symmetric chest plumage.Proc R Soc B258267271
  9. 9. Gonzalez G, Sorci G, Smith LC, de Lope F (2001) Testosterone and sexual signalling in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 50: 557–62.G. GonzalezG. SorciLC SmithF. de Lope2001Testosterone and sexual signalling in male house sparrows (Passer domesticus).Behav Ecol Sociobiol5055762
  10. 10. Dixson BJ, Dixson AF, Bishop P, Parish A (2010) Human physique and sexual attractiveness in men and women: a New Zealand–U.S.A comparative study. Arch Sex Behav 39: 798–806.BJ DixsonAF DixsonP. BishopA. Parish2010Human physique and sexual attractiveness in men and women: a New Zealand–U.S.A comparative study.Arch Sex Behav39798806
  11. 11. Møller AP, Soler M, Thornhill R (1995) Breast asymmetry, sexual selection, and human reproductive success. Ethol Sociobiol 16: 207–219.AP MøllerM. SolerR. Thornhill1995Breast asymmetry, sexual selection, and human reproductive success.Ethol Sociobiol16207219
  12. 12. Singh D, Young RK (1995) Body weight, waist-to-hip ratio, breasts, and hips: role in judgments of female attractiveness and desirability for relationships. Ethol Sociobiol 16: 483–507.D. SinghRK Young1995Body weight, waist-to-hip ratio, breasts, and hips: role in judgments of female attractiveness and desirability for relationships.Ethol Sociobiol16483507
  13. 13. Morris D (1967) The naked ape. New York: Delta Press. 256 p.D. Morris1967The naked apeNew YorkDelta Press256
  14. 14. Darwin C (1871) The descent of man and selection in relation to sex. London: John Murray. C. Darwin1871The descent of man and selection in relation to sexLondonJohn Murray
  15. 15. Bigoni F, Stanyon R (2010) L'antropologia e la teoria della selezione sessuale: da Darwin e Mantegazza ad oggi. Archivio per l'Antropologia e la Etnologia CXL 7–20.F. BigoniR. Stanyon2010L'antropologia e la teoria della selezione sessuale: da Darwin e Mantegazza ad oggi.Archivio per l'Antropologia e la Etnologia CXL720
  16. 16. Kappeler PM, van Schaik C (2004) Sexual selection in primates. Cambridge: Cambridge University Press. UK. 284 p.PM KappelerC. van Schaik2004Sexual selection in primatesCambridgeCambridge University Press. UK284
  17. 17. Fleagle JG (1999) Primate adaptation and evolution, 2nd ed. San Diego: Academic Press. 596 p.JG Fleagle1999Primate adaptation and evolution, 2nd edSan DiegoAcademic Press596
  18. 18. Utami Atmoko S, van Hooff JARAM (2004) Alternative male reproductive strategies: male bimaturism in orangutans. In: Kappeler PM, van Schaik CP, editors. Sexual selection in primates: new and comparative perspectives. pp. 196–207.S. Utami AtmokoJARAM van Hooff2004Alternative male reproductive strategies: male bimaturism in orangutans.PM KappelerCP van SchaikSexual selection in primates: new and comparative perspectives196207Cambridge University Press, Cambridge. Cambridge University Press, Cambridge.
  19. 19. Utami SS, Goossens B, Bruford MW, de Ruiter JR, van Hooff JARAM (2002) Male bimaturism and reproductive success in Sumatran orang-utans. Behav Ecol 13: 643–652.SS UtamiB. GoossensMW BrufordJR de RuiterJARAM van Hooff2002Male bimaturism and reproductive success in Sumatran orang-utans.Behav Ecol13643652
  20. 20. Jolly A (1966) Lemur behavior: a Madagascar field study. Chicago: University of Chicago Press. A. Jolly1966Lemur behavior: a Madagascar field studyChicagoUniversity of Chicago Press
  21. 21. Brockman DK (1999) Reproductive behavior of female Propithecus verreauxi at Beza Mahafaly, Madagascar. Int J Primatol 20: 375–398.DK Brockman1999Reproductive behavior of female Propithecus verreauxi at Beza Mahafaly, Madagascar.Int J Primatol20375398
  22. 22. Norscia I, Antonacci D, Palagi E (2009) Mating First, Mating More: Biological Market Fluctuation in a Wild Prosimian. PLoS ONE 4(3): e4679.I. NorsciaD. AntonacciE. Palagi2009Mating First, Mating More: Biological Market Fluctuation in a Wild Prosimian.PLoS ONE43e4679
  23. 23. Richard AF (1992) Aggressive competition between males, female-controlled polygyny and sexual monomorphism in a Malagasy primate, Propithecus verreauxi. J Hum Evol 22: 395–406.AF Richard1992Aggressive competition between males, female-controlled polygyny and sexual monomorphism in a Malagasy primate, Propithecus verreauxi.J Hum Evol22395406
  24. 24. Lewis RJ (2002) Beyond dominance: the importance of leverage. Quarterly Review of Biology 77: 149–164.RJ Lewis2002Beyond dominance: the importance of leverage.Quarterly Review of Biology77149164
  25. 25. Lewis RJ (2005) Sex differences in scent-marking in sifaka: mating conflict or male services? Am J Phys Anthropol 128: 389–398.RJ Lewis2005Sex differences in scent-marking in sifaka: mating conflict or male services?Am J Phys Anthropol128389398
  26. 26. Lewis RJ, van Schaik CP (2007) Bimorphism in male Verreaux' sifaka in the Kirindy forest of Madagascar. Int J Primatol 28: 159–182.RJ LewisCP van Schaik2007Bimorphism in male Verreaux' sifaka in the Kirindy forest of Madagascar.Int J Primatol28159182
  27. 27. Pochron ST, Morelli TL, Terranova P, Scirbona J, Cohen J (2005) Patterns of male scent marking in Propithecus edwardsi of Ranomafana National Park, Madagascar. Am J Primatol 65: 103–115.ST PochronTL MorelliP. TerranovaJ. ScirbonaJ. Cohen2005Patterns of male scent marking in Propithecus edwardsi of Ranomafana National Park, Madagascar.Am J Primatol65103115
  28. 28. Mertl-Millhollen AS (2006) Scent marking as resource defense by female Lemur catta. Am J Primatol 68: 605–621.AS Mertl-Millhollen2006Scent marking as resource defense by female Lemur catta.Am J Primatol68605621
  29. 29. Kappeler PM (1990) Social status and scent-marking behaviour in Lemur catta. Anim Behav 40: 774–775.PM Kappeler1990Social status and scent-marking behaviour in Lemur catta.Anim Behav40774775
  30. 30. Palagi E, Telara S, Borgognini Tarli S (2003) Sniffing behaviour in Lemur catta: seasonality, sex, and rank. Int J Primatol 24: 335–350.E. PalagiS. TelaraS. Borgognini Tarli2003Sniffing behaviour in Lemur catta: seasonality, sex, and rank.Int J Primatol24335350
  31. 31. Palagi E, Telara S, Borgognini Tarli S (2004) Reproductive strategies in Lemur catta: the balance among sending, receiving, and countermarking scent signals. Int J Primatol 25: 1019–1031.E. PalagiS. TelaraS. Borgognini Tarli2004Reproductive strategies in Lemur catta: the balance among sending, receiving, and countermarking scent signals.Int J Primatol2510191031
  32. 32. Fisher HS, Swaisgood RR, Fitch-Snyder H (2003) Countermarking by male pygmy lorises (Nycticebus pygmaeus): do females use odour cues to select mates with high competitive ability? Behav Ecol Sociobiol 53: 123–130.HS FisherRR SwaisgoodH. Fitch-Snyder2003Countermarking by male pygmy lorises (Nycticebus pygmaeus): do females use odour cues to select mates with high competitive ability?Behav Ecol Sociobiol53123130
  33. 33. Lewis RJ (2009) Chest staining variation as a signal of testosterone levels in male Verreaux's sifaka. Physiol Behav 96: 586–592.RJ Lewis2009Chest staining variation as a signal of testosterone levels in male Verreaux's sifaka.Physiol Behav96586592
  34. 34. Wong BBM, Candolin U (2005) How is female mate choice affected by male competition? Biol Rev 80: 559–571.BBM WongU. Candolin2005How is female mate choice affected by male competition?Biol Rev80559571
  35. 35. Noë R, Hammerstein P (1995) Biological markets. Trends Ecol Evol 10: 336–340.R. NoëP. Hammerstein1995Biological markets.Trends Ecol Evol10336340
  36. 36. Coleman SW, Patricelli GL, Borgia G (2004) Variable female preferences drive complex male displays. Nature 428: 742–745.SW ColemanGL PatricelliG. Borgia2004Variable female preferences drive complex male displays.Nature428742745
  37. 37. Blaustein AR (1981) Sexual selection and mammalian olfaction. Am Nat 117: 1006–1010.AR Blaustein1981Sexual selection and mammalian olfaction.Am Nat11710061010
  38. 38. McNamara JM, Barta Z, Fromhage L, Houston AI (2008) The coevolution of choosiness and cooperation. Nature 451: 189–192.JM McNamaraZ. BartaL. FromhageAI Houston2008The coevolution of choosiness and cooperation.Nature451189192
  39. 39. Hemelrijk CK, Steinhauser J (2007) Cooperation, coalition, and alliances. In: Henk W, Tattersall I, eds. Handbook of Paleoanthropology, Part II. Berlin: Springer 1321–1346.CK HemelrijkJ. Steinhauser2007Cooperation, coalition, and alliances. In: Henk W, Tattersall I, eds. Handbook of Paleoanthropology, Part II.Berlin: Springer13211346
  40. 40. Antonacci D, Norscia I, Palagi E (2010) Stranger to familiar: wild strepsirhines manage xenophobia by playing. PloS ONE 5(10): e13218.D. AntonacciI. NorsciaE. Palagi2010Stranger to familiar: wild strepsirhines manage xenophobia by playing.PloS ONE510e13218
  41. 41. Thiessen D, Rice M (1976) Mammalian scent gland marking and social behavior. Psychol Bull 83: 505–539.D. ThiessenM. Rice1976Mammalian scent gland marking and social behavior.Psychol Bull83505539
  42. 42. Zala SM, Potts WK, Penn DJ (2004) Scent-marking displays provide honest signals of health and infection. Behav Ecol 15: 338–344.SM ZalaWK PottsDJ Penn2004Scent-marking displays provide honest signals of health and infection.Behav Ecol15338344
  43. 43. Macrides F, Bartke A, Dalterio S (1975) Strange females increase plasma testosterone levels in male mice. Science 189: 1104–1106.F. MacridesA. BartkeS. Dalterio1975Strange females increase plasma testosterone levels in male mice.Science18911041106
  44. 44. Lawler RR (2007) Fitness and extra-group reproduction in male Verreaux's sifaka: an analysis of reproductive success from 1989–1999. Am J Phys Anthropol 132: 267–277.RR Lawler2007Fitness and extra-group reproduction in male Verreaux's sifaka: an analysis of reproductive success from 1989–1999.Am J Phys Anthropol132267277
  45. 45. Rowe C (1999) Receiver psychology and the evolution of multicomponent signals. Anim Behav 58: 921–931.C. Rowe1999Receiver psychology and the evolution of multicomponent signals.Anim Behav58921931
  46. 46. Kappeler PM (1998) To whom it may concern: the transmission and function of chemical signals in Lemur catta. Behav Ecol Sociobiol 42: 411–421.PM Kappeler1998To whom it may concern: the transmission and function of chemical signals in Lemur catta.Behav Ecol Sociobiol42411421
  47. 47. Guilford T, Dawkins MS (1991) Receiver psychology and the evolution of animal signals. Anim Behav 42: 1–14.T. GuilfordMS Dawkins1991Receiver psychology and the evolution of animal signals.Anim Behav42114
  48. 48. Rowe C, Guilford T (1999) Novelty in a multimodal warning signal. Anim Behav 57: 341–346.C. RoweT. Guilford1999Novelty in a multimodal warning signal.Anim Behav57341346
  49. 49. Palagi E, Dapporto L, Borgognini Tarli S (2005) The neglected scent: on the marking function of urine in Lemur catta. Behav Ecol Sociobiol 58: 437–445.E. PalagiL. DapportoS. Borgognini Tarli2005The neglected scent: on the marking function of urine in Lemur catta.Behav Ecol Sociobiol58437445
  50. 50. Drea CM, Scordato ES (2008) Olfactory communication in the ringtailed lemur (Lemur catta): form and function of multimodal signals. In: Jane L, Hurst JL, Beynon RJ, Roberts SC, Wyatt TD, editors. Chemical signals in vertebrates, Vol. 11. New York: Springer. pp. 91–102.CM DreaES Scordato2008Olfactory communication in the ringtailed lemur (Lemur catta): form and function of multimodal signals.L. JaneJL HurstRJ BeynonSC RobertsTD WyattChemical signals in vertebrates, Vol. 11New YorkSpringer91102
  51. 51. Buesching CD, Heistermann M, Hodges JK, Zimmermann E (1998) Multimodal oestrus advertisement in a small nocturnal prosimian, Microcebus murinus. Folia Primatol 69: 295–308.CD BueschingM. HeistermannJK HodgesE. Zimmermann1998Multimodal oestrus advertisement in a small nocturnal prosimian, Microcebus murinus.Folia Primatol69295308
  52. 52. Pochron ST, Wright PC (2003) Variability in adult group compositions of a prosimian primate. Behav Ecol Sociobiol 54: 285–293.ST PochronPC Wright2003Variability in adult group compositions of a prosimian primate.Behav Ecol Sociobiol54285293
  53. 53. Palagi E, Dapporto L (2006) Urine marking and urination in Lemur catta: a comparison of design features. Ann Zool Fenn 43: 280–284.E. PalagiL. Dapporto2006Urine marking and urination in Lemur catta: a comparison of design features.Ann Zool Fenn43280284
  54. 54. Henzi SP, Barrett L (1999) The value of grooming to female primates. Primates 40: 47–59.SP HenziL. Barrett1999The value of grooming to female primates.Primates404759
  55. 55. Gumert MD (2006) Payment for sex in a macaque mating market. Anim Behav 74: 1655–1667.MD Gumert2006Payment for sex in a macaque mating market.Anim Behav7416551667
  56. 56. Stopka P, Johnson DDP, Barrett L (2001) ‘Friendship’ for fitness or ‘friendship’ for friendship's sake? Anim Behav 61: F19–F21.P. StopkaDDP JohnsonL. Barrett2001‘Friendship’ for fitness or ‘friendship’ for friendship's sake?Anim Behav61F19F21
  57. 57. Kappeler PM, Schäffler L (2008) The lemur syndrome unresolved: extreme male reproductive skew in sifakas (Propithecus verreauxi), a sexually monomorphic primate with female dominance. Behav Ecol Sociobiol 62: 1007–1015.PM KappelerL. Schäffler2008The lemur syndrome unresolved: extreme male reproductive skew in sifakas (Propithecus verreauxi), a sexually monomorphic primate with female dominance.Behav Ecol Sociobiol6210071015
  58. 58. Norscia I, Palagi E (2011) Fragment quality and distribution of the arboreal primate Propithecus verreauxi in the spiny forest of South Madagascar. J Trop Ecol 27: 103–106.I. NorsciaE. Palagi2011Fragment quality and distribution of the arboreal primate Propithecus verreauxi in the spiny forest of South Madagascar.J Trop Ecol27103106
  59. 59. Jolly A, Koyama N, Rasamimanana H, Crowley H, Williams G (2006) Berenty Reserve: A research site in southern Madagascar. In: Jolly A, Sussman RW, Koyama N, Rasamimanana H, editors. Ringtailed lemur biology: Lemur catta in Madagascar. New York: Springer Verlag Press. pp. 32–42.A. JollyN. KoyamaH. RasamimananaH. CrowleyG. Williams2006Berenty Reserve: A research site in southern Madagascar.A. JollyRW SussmanN. KoyamaH. RasamimananaRingtailed lemur biology: Lemur catta in MadagascarNew YorkSpringer Verlag Press3242
  60. 60. Norscia I, Palagi E (2008) Berenty 2006: census of Propithecus verreauxi and possible evidence of population stress. Int J Primatol 29: 1099–1115.I. NorsciaE. Palagi2008Berenty 2006: census of Propithecus verreauxi and possible evidence of population stress.Int J Primatol2910991115
  61. 61. Tattersall I (1982) The Primates of Madagascar. New York: Columbia University Press. 382 p.I. Tattersall1982The Primates of MadagascarNew YorkColumbia University Press382
  62. 62. Jolly A (1972) Troop continuity and troop spacing in Propithecus verreauxi and Lemur catta at Berenty (Madagascar). Folia Primatol 17: 335–362.A. Jolly1972Troop continuity and troop spacing in Propithecus verreauxi and Lemur catta at Berenty (Madagascar).Folia Primatol17335362
  63. 63. Manly BFJ (1997) Randomization, bootstrap and Montecarlo methods in biology. London: Chapman and Hall. BFJ Manly1997Randomization, bootstrap and Montecarlo methods in biologyLondonChapman and Hall