Physiological Suppression of Sexual Function of Subordinate MalesA Subtle Form of Intrasexual Competition Among Male Sifakas (Propithecus verreauxi)?

Kraus, Cornelia; Heistermann, Michael; Kappeler, Peter M.

doi:10.1016/s0031-9384(99)00024-4

Cited by 128 publications

(126 citation statements)

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“…In the last three of these species, the VNO is not involved in all of the functions mediated by the rodent VNO (CohenTannoudji et al, 1989;Dorries et al, 1997;Weiler, et al, 1999;Kelliher et al, 2001). Likewise, several behaviors that in rodents are mediated by the VNO are not solely VNO-mediated in primates (Barrett et al, 1993;Aujard, 1997;Kraus et al, 1999). The histological similarities to sheep, swine, and ferret VNO together with the behavioral observations argue that primate VNO function is likely to be restricted compared to rodents and more similar to that of the former species.…”

Section: Discussionmentioning

confidence: 99%

Expression of neuron‐specific markers by the vomeronasal neuroepithelium in six species of primates

et al. 2004

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Vomeronasal organ (VNO) morphology varies markedly across primate taxa. Old World monkeys display no postnatal VNO. Humans and at least some apes retain a vestigial VNO during postnatal life, whereas the strepsirrhines and New World Monkeys present a morphologically well-defined VNO that, in many species, is presumed to function as an olfactory organ. Available microanatomical and behavioral studies suggest that VNO function in these species does not precisely duplicate that described in other mammalian taxa. The questions of which species retain a functional VNO and what functions they serve require inquiry along diverse lines but, to be functional, the vomeronasal epithelium must be neuronal and olfactory. We used immunohistochemistry to establish these criteria in six primate species. We compared the expression of two neuronal markers, neuron-specific ␤-tubulin (BT) and protein gene product 9.5, and olfactory marker protein (OMP), a marker of mature olfactory sensory neurons, in paraffin-embedded VNO sections from two strepsirrhine and four haplorhine species, all of which retain morphologically well-defined VNOs during postnatal life. The infant Eulemur mongoz, adult Otolemur crassicaudatus, neonatal Leontopithicus rosalia, and adult Callithrix jacchus express all three proteins in their well-defined vomeronasal neuroepithelia. The infant Tarsius syrichta showed some BT and OMP immunoreactivity. We establish that two strepsirrhine species and at least some New World haplorhines have mature sensory neurons in the VNO. In contrast, at all ages examined, Saguinus geoffroyi VNO expresses these markers in only a few cells. © 2004 Wiley-Liss, Inc.Key words: immunohistochemistry; olfaction; olfactory marker protein; primate; ␤-tubulin; PGP 9.5; vomeronasalThe tetrapod vomeronasal organ (VNO) is bilaterally symmetric and lies along the ventrorostral aspect of the nasal septum. Sensory neurons in the vomeronasal neuroepithelium (VNNE) of snakes, rodents, and opossums detect chemical signals that evoke behavioral and/or physiological changes regarding prey identification, social status, and reproductive state (Wysocki, 1979;Halpern, 1987;Takami, 2002;Halpern and Martínez-Marcos, 2003).The rodent VNO is the best studied in terms of gene expression during development, its morphological organization, its secondary and higher-order connections, and its effects on the organism's behavior and physiology. For some time, the rodent VNO was thought to epitomize the mammalian vomeronasal system but VNO function as exemplified in rodents is not precisely replicated in other mammalian taxa, namely, ferrets (Weiler et al., 1999;

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Section: Discussionmentioning

confidence: 99%

Expression of neuron‐specific markers by the vomeronasal neuroepithelium in six species of primates

et al. 2004

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“…The faecal and saliva samples were measured for immunoreactive testosterone by microtitreplate enzyme immunoassays following previously established methods (Kraus et al 1999). Two di¡erent antisera were used, one of which was purchased from Dr E. Mo« stl (Veterinary University of Vienna, Austria) and the second (BioClin) from BioClinical Services Ltd (Cardi¡, UK).…”

Section: (C) Sample Collection and Hormone Analysismentioning

confidence: 99%

“…The samples were diluted in assay bu¡er for the hormone assay (for details see Kraus et al 1999) and 50 m l aliquots of standards, controls and unknowns were pipetted in duplicate into the microtitreplate wells. Fifty microlitres biotinylated testosterone label and 50 m l antiserum were added and the plates incubated overnight at 4 8C.…”

Section: (C) Sample Collection and Hormone Analysismentioning

confidence: 99%

“…We measured their androgen concentrations in faeces and saliva before and during the mating season using non-invasive sampling methods. Hormone measurements in faeces are an established approach to studying the interaction of hormones and behaviour in lemurs (Brockman et al 1998;Cavigelli 1999;Kraus et al 1999). In addition, we examined the relationship between androgen levels and female rank within the female hierarchy, rates of con£icts and rates of aggression, respectively.…”

Section: Introductionmentioning

confidence: 99%

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Androgen levels and female social dominance inLemur catta

Engelhard

Kappeler

Heistermann

2000

Proc. R. Soc. Lond. B

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Morphological and behavioural traits which improve agonistic power are subject to intrasexual selection and, at the proximate level, are in£uenced by circulating androgens. Because intrasexual selection in mammals is more intense among males, they typically dominate females. Female social dominance is therefore unexpected and, indeed, rare. Ring-tailed lemurs (Lemur catta) are sexually monomorphic primates in which all adult females dominate all males. The goal of our study was to test the prediction that female dominance in this species is associated with high androgen levels. Using two captive groups, we collected data on agonistic behaviour and non-invasively assessed their androgen concentrations in faeces and saliva by enzyme immunoassay. We found that adult female L. catta do not have higher androgen levels than males. However, during the mating season there was a twofold increase in both the androgen levels and con£ict rates among females. This seasonal increase in their androgen levels was probably not due to a general increase in ovarian hormone production because those females showing the strongest signs of follicular development tended to have low androgen concentrations. At the individual level neither the individual aggression rates nor the proportion of same-sexed individuals dominated were correlated with their androgen levels. We conclude that female dominance in ring-tailed lemurs is neither based on physical superiority nor on high androgen levels and that it is equally important to study male subordination and prenatal brain priming e¡ects for a complete understanding of this phenomenon.

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“…Infanticide by strange males following group takeovers is another male reproductive strategy (Lewis et al 2003). One male in each group is dominant, has a large chest gland, and has significantly elevated testosterone levels during the mating season (Kraus et al 1999;Lewis and van Schaik 2007), but there is no directional selection on male body mass or canine size (Lawler et al 2005). However, because access to receptive females is independent of the occurrence or outcome of male aggression and may be mediated in part by sperm competition (see Pochron and Wright 2005), the sifaka mating system has been characterized as female-controlled polygyny (Richard 1992).…”

Section: Introductionmentioning

confidence: 99%

The lemur syndrome unresolved: extreme male reproductive skew in sifakas (Propithecus verreauxi), a sexually monomorphic primate with female dominance

Kappeler

Schäffler

2007

Behav Ecol Sociobiol

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The primates of Madagascar (Lemuriformes) are unusual among mammals in that polygynous species lack sexual dimorphism, and females dominate males socially in most species. Moreover, lemur groups are relatively small and characterized by even adult sex ratios despite the fact that one male should be able to exclude other males from the group. One hypothesis to explain this combination of behavioral, morphological, and demographic traits (the "lemur syndrome") postulates that male-male competition is relaxed and, hence, variance in male reproductive success is low. Reproductive skew theory provides a framework for testing this and several related predictions about lemur social evolution. Specifically, low reproductive skew is also predicted if dominant males or adult females make reproductive concessions to subordinates or if the latter group successfully pursues alternative reproductive tactics. However, suitable data on paternity, demography, and behavior for a conclusive test of these predictions have not been available in the past. In this paper, we show that male reproductive success in ten groups of Verreaux's sifakas (Propithecus verreauxi) was extremely skewed in favor of the dominant male over 9 years. Our genetic analyses also revealed that more than a third of all groups are effectively harem groups because only one male was unrelated to the resident female(s). In groups with two or more non-natal males, the dominant sired 91% of 33 infants. Together, males pursuing one of several alternative reproductive tactics, such as roaming among several groups or immigrating peacefully, sired only 11% of infants. Thus, female sifakas do not control group composition by offering reproductive opportunities to subordinate males as staying incentives, intrasexual selection is not relaxed, and dominant males prevail in a tug-of-war over subordinate males. Because male reproductive skew in sifakas is even more pronounced than in harem-living anthropoids studied to date, intrasexual selection is clearly not relaxed, and the lemur syndrome is more puzzling than ever.

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Physiological Suppression of Sexual Function of Subordinate MalesA Subtle Form of Intrasexual Competition Among Male Sifakas (Propithecus verreauxi)?

Cited by 128 publications

References 44 publications

Expression of neuron‐specific markers by the vomeronasal neuroepithelium in six species of primates

Expression of neuron‐specific markers by the vomeronasal neuroepithelium in six species of primates

Androgen levels and female social dominance inLemur catta

The lemur syndrome unresolved: extreme male reproductive skew in sifakas (Propithecus verreauxi), a sexually monomorphic primate with female dominance

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