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Plasma Testosterone and Androstenedione Levels Follow the Same Sex-Specific Patterns in the Two Pan Species

SIMPLE SUMMARY: Generally male mammals are more aggressive than their female peers. In these males, aggressive behavior is linked to levels of androgens; higher levels of testosterone are predictive of higher aggression rates or more severe aggression. There are some species where the pattern of sex...

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Autores principales: Sonnweber, Ruth, Stevens, Jeroen M. G., Hohmann, Gottfried, Deschner, Tobias, Behringer, Verena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9495489/
https://www.ncbi.nlm.nih.gov/pubmed/36138754
http://dx.doi.org/10.3390/biology11091275
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author Sonnweber, Ruth
Stevens, Jeroen M. G.
Hohmann, Gottfried
Deschner, Tobias
Behringer, Verena
author_facet Sonnweber, Ruth
Stevens, Jeroen M. G.
Hohmann, Gottfried
Deschner, Tobias
Behringer, Verena
author_sort Sonnweber, Ruth
collection PubMed
description SIMPLE SUMMARY: Generally male mammals are more aggressive than their female peers. In these males, aggressive behavior is linked to levels of androgens; higher levels of testosterone are predictive of higher aggression rates or more severe aggression. There are some species where the pattern of sex-specific aggression is reversed, and it was hypothesized that high levels of androgens may be responsible for social dominance and aggressiveness in these females. Studies so far found that females of species with sex-reversed aggression patterns (e.g., spotted hyenas and ring-tailed lemurs) had lower plasma testosterone levels than their male peers, but a precursor of testosterone, androstenedione, was comparable or even higher in females than in males. This supported the idea that selection for female aggressiveness may be facilitated through augmented androgen secretion. Here we show that in two sister species, bonobos and chimpanzees, that differ in terms of sex-specific aggression patterns, females have lower plasma testosterone levels and higher plasma androstenedione levels than their male peers. Thus, our data do not support a theory of a role of female androgen levels on the expression of sex-specific patterns of aggression. ABSTRACT: In most animals, males are considered more aggressive, in terms of frequency and intensity of aggressive behaviors, than their female peers. However, in several species this widespread male-biased aggression pattern is either extenuated, absent, or even sex-reversed. Studies investigating potential neuro-physiological mechanisms driving the selection for female aggression in these species have revealed an important, but not exclusive role of androgens in the expression of the observed sex-specific behavioral patterns. Two very closely related mammalian species that markedly differ in the expression and degree of sex-specific aggression are the two Pan species, where the chimpanzee societies are male-dominated while in bonobos sex-biased aggression patterns are alleviated. Using liquid chromatography–mass spectrometry (LC-MS) methods, we measured levels of plasma testosterone and androstenedione levels in male and female zoo-housed bonobos (N = 21; 12 females, 9 males) and chimpanzees (N = 41; 27 females, 14 males). Our results show comparable absolute and relative intersexual patterns of blood androgen levels in both species of Pan. Plasma testosterone levels were higher in males (bonobos: females: average 0.53 ± 0.30 ng/mL; males 6.70 ± 2.93 ng/mL; chimpanzees: females: average 0.40 ± 0.23 ng/mL; males 5.84 ± 3.63 ng/mL) and plasma androstenedione levels were higher in females of either species (bonobos: females: average 1.83 ± 0.87 ng/mL; males 1.13 ± 0.44 ng/mL; chimpanzees: females: average 1.84 ± 0.92 ng/mL; males 1.22 ± 0.55 ng/mL). The latter result speaks against a role of androstenedione in the mediation of heightened female aggression, as had been suggested based on studies in other mammal species where females are dominant and show high levels of female aggressiveness.
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spelling pubmed-94954892022-09-23 Plasma Testosterone and Androstenedione Levels Follow the Same Sex-Specific Patterns in the Two Pan Species Sonnweber, Ruth Stevens, Jeroen M. G. Hohmann, Gottfried Deschner, Tobias Behringer, Verena Biology (Basel) Article SIMPLE SUMMARY: Generally male mammals are more aggressive than their female peers. In these males, aggressive behavior is linked to levels of androgens; higher levels of testosterone are predictive of higher aggression rates or more severe aggression. There are some species where the pattern of sex-specific aggression is reversed, and it was hypothesized that high levels of androgens may be responsible for social dominance and aggressiveness in these females. Studies so far found that females of species with sex-reversed aggression patterns (e.g., spotted hyenas and ring-tailed lemurs) had lower plasma testosterone levels than their male peers, but a precursor of testosterone, androstenedione, was comparable or even higher in females than in males. This supported the idea that selection for female aggressiveness may be facilitated through augmented androgen secretion. Here we show that in two sister species, bonobos and chimpanzees, that differ in terms of sex-specific aggression patterns, females have lower plasma testosterone levels and higher plasma androstenedione levels than their male peers. Thus, our data do not support a theory of a role of female androgen levels on the expression of sex-specific patterns of aggression. ABSTRACT: In most animals, males are considered more aggressive, in terms of frequency and intensity of aggressive behaviors, than their female peers. However, in several species this widespread male-biased aggression pattern is either extenuated, absent, or even sex-reversed. Studies investigating potential neuro-physiological mechanisms driving the selection for female aggression in these species have revealed an important, but not exclusive role of androgens in the expression of the observed sex-specific behavioral patterns. Two very closely related mammalian species that markedly differ in the expression and degree of sex-specific aggression are the two Pan species, where the chimpanzee societies are male-dominated while in bonobos sex-biased aggression patterns are alleviated. Using liquid chromatography–mass spectrometry (LC-MS) methods, we measured levels of plasma testosterone and androstenedione levels in male and female zoo-housed bonobos (N = 21; 12 females, 9 males) and chimpanzees (N = 41; 27 females, 14 males). Our results show comparable absolute and relative intersexual patterns of blood androgen levels in both species of Pan. Plasma testosterone levels were higher in males (bonobos: females: average 0.53 ± 0.30 ng/mL; males 6.70 ± 2.93 ng/mL; chimpanzees: females: average 0.40 ± 0.23 ng/mL; males 5.84 ± 3.63 ng/mL) and plasma androstenedione levels were higher in females of either species (bonobos: females: average 1.83 ± 0.87 ng/mL; males 1.13 ± 0.44 ng/mL; chimpanzees: females: average 1.84 ± 0.92 ng/mL; males 1.22 ± 0.55 ng/mL). The latter result speaks against a role of androstenedione in the mediation of heightened female aggression, as had been suggested based on studies in other mammal species where females are dominant and show high levels of female aggressiveness. MDPI 2022-08-27 /pmc/articles/PMC9495489/ /pubmed/36138754 http://dx.doi.org/10.3390/biology11091275 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Sonnweber, Ruth
Stevens, Jeroen M. G.
Hohmann, Gottfried
Deschner, Tobias
Behringer, Verena
Plasma Testosterone and Androstenedione Levels Follow the Same Sex-Specific Patterns in the Two Pan Species
title Plasma Testosterone and Androstenedione Levels Follow the Same Sex-Specific Patterns in the Two Pan Species
title_full Plasma Testosterone and Androstenedione Levels Follow the Same Sex-Specific Patterns in the Two Pan Species
title_fullStr Plasma Testosterone and Androstenedione Levels Follow the Same Sex-Specific Patterns in the Two Pan Species
title_full_unstemmed Plasma Testosterone and Androstenedione Levels Follow the Same Sex-Specific Patterns in the Two Pan Species
title_short Plasma Testosterone and Androstenedione Levels Follow the Same Sex-Specific Patterns in the Two Pan Species
title_sort plasma testosterone and androstenedione levels follow the same sex-specific patterns in the two pan species
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9495489/
https://www.ncbi.nlm.nih.gov/pubmed/36138754
http://dx.doi.org/10.3390/biology11091275
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