Sexual dimorphism in postcranial skeletal shape suggests male‐biased specialization for physical competition in anthropoid primates

Abstract

Sexual dimorphism often arises as a response to selection on traits that improve a male's ability to physically compete for access to mates. In primates, sexual dimorphism in body mass and canine size is more common in species with intense male–male competition. However, in addition to these traits, other musculoskeletal adaptations may improve male fighting performance. Postcranial traits that increase strength, agility, and maneuverability may also be under selection. To test the hypothesis that males, as compared to females, are more specialized for physical competition in their postcranial anatomy, we compared sex‐specific skeletal shape using a set of functional indices predicted to improve fighting performance. Across species, we found significant sexual dimorphism in a subset of these indices, indicating the presence of skeletal shape sexual dimorphism in our sample of anthropoid primates. Mean skeletal shape sexual dimorphism was positively correlated with sexual dimorphism in body size, an indicator of the intensity of male–male competition, even when controlling for both body mass and phylogenetic relatedness. These results suggest that selection on male fighting ability has played a role in the evolution of postcranial sexual dimorphism in primates.

Musculoskeletal mass and shape are correlated with competitive ability in male house mice (Mus musculus)

“…For postcranial measurements, we used physiological length, which is defined as the length between articular surfaces and represents the effective working length of a bone (Wilder, 1920). From this set of 18 morphometrics, we calculated 12 functional indices (Table 3) that quantify skeletal shape in the form of relative proportions, robusticity and anatomical mechanical advantage (Morris and Brandt, 2014;Morris and Carrier, 2016;Morris et al, 2019). These skeletal indices represent a set of traits hypothesized to be associated with improved fighting performance, with larger ratio values suggesting greater anatomical specialization for fighting performance.…”

“…See Table 2 for description of skeletal morphometrics. Morris and Brandt (2014), Morris and Carrier (2016) and Morris et al (2019).…”

“…Head size morphometrics in relation to biting performance have been intensely studied (in mammals: Hanski et al, 1991;Koren et al, 2008;in lizards: Hews, 1990;Olsson, 1994;Molina-Borja et al, 1998;Alberts et al, 2002;López and Martín, 2002;Gier, 2003;Lailvaux et al, 2004;Perry et al, 2004;Huyghe et al, 2005;Lappin and Husak, 2005;Husak et al, 2006;Kohlsdorf et al, 2006;Stuart-Fox et al, 2006;Whiting et al, 2006;Stuart-Fox et al, 2009;Huyghe et al, 2012;Cameron et al, 2013;McEvoy et al, 2013;McLean and Stuart-Fox, 2015;Bush et al, 2016;Fernández et al, 2018). In several species, male-biased sexual dimorphism has been identified in muscle mass, limb length and skeletal shape indices associated with anatomical specialization for fighting performance (in primates: Gallagher et al, 1997;Zihlman and McFarland, 2000;Nindl et al, 2002, Abe et al, 2003Lassek and Gaulin, 2009;Morris et al, 2019;in macropodids: Jarman, 1983in macropodids: Jarman, , 1989Warburton et al, 2013;Richards et al, 2015;in carnivores: Pasi and Carrier, 2003;Kemp et al, 2005;Morris and Brandt, 2014;Morris and Carrier, 2016), but these studies did not directly measure the correlation between these characters and the outcome of male-male contests. In suc...…”

“…Therefore, individuals with relatively larger muscle mass will be capable of producing more force and power, permitting them to more easily manipulate an opponent. Our second aim was to investigate whether winners possessed greater bone mass and other sets of skeletal shape adaptations consistent with specialization for physical competition (Morris and Brandt, 2014;Morris and Carrier, 2016;Morris et al, 2019). Overall, we expected the bones of winners to be more robust and, therefore, heavier than those of their less-competitive counterparts.…”

Patterns of recent natural selection on genetic loci associated with sexually differentiated human body size and shape phenotypes

“…In species with high inter-male competition for mates, larger males may have a competitive advantage that results in increased fitness (Plavcan, 2001). Perhaps as a result, the magnitude of sexually differentiated phenotypes are often greater in polygynous species with high competition (e.g., gorillas) and lower in monogamous species (e.g., gibbons) (Lindenfors & Tullberg, 1998;Morris, Cunningham, & Carrier, 2019;Plavcan, 2001). Large ranges in the degree of body size and shape sexually differentiated traits are repeatedly observed among closely related groups of species, suggesting the potential for relatively rapid evolution (Plavcan, 2001).…”