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Musculoskeletal mass and shape are correlated with competitive ability in male house mice (Mus musculus) RESEARCH ARTICLE Musculoskeletal mass and shape are correlated with competitive ability in male house mice (Mus musculus) Amanda N. Cooper1,*, Christopher B. Cunningham2, Jeremy S. Morris3, James S. Ruff1, Wayne K. Potts1 and David R. Carrier1 ABSTRACT Intense physical competition betweenmales for mating opportunities is widespread among mammals. In such agonistic encounters, males with combinations of morphological, physiological and behavioral characters that allow them to dominate an opponent have greater fitness. However, the specific physical traits associated with competitive ability are poorly understood. Larger body size is often correlated with fitness in mammals. Interestingly, fitness is maximized at intermediate body masses in male house mice (Mus musculus), a species with a polygynous mating system in which males compete physically for access to reproductive resources. Here, we used competition trials in semi-natural, mixed-sex population enclosures to directly measure competitive ability in male house mice based on control of a preferred nesting site. We tested the hypothesis that the musculoskeletal systems of malemice demonstrating high competitive ability are more specialized for competition by comparing the masses of 10 major muscle groups and eight bones as well as a set of 12 skeletal shape indices associated with anatomical specialization for fighting performance in a set of nine winners and 20 losers. Winning males possessed several traits hypothesized to enhance performance in male–male contests: relatively greater mass in several muscle groups and bones of the forelimb and hindlimb and larger scapular surface area. Unexpectedly, no measurements of the head and neck differed significantly between winners and losers. These results identify musculoskeletal traits associated with competitive ability in male house mice and suggest that our current understanding of mammalian fighting performance is incomplete and more nuanced than previously considered. KEY WORDS: Biomechanics, Life-history traits, Morphology, Musculoskeletal system, Sexual selection INTRODUCTION The outcome of agonistic encounters is directly associated with reproductive fitness for males of many mammalian species (Dewsbury, 1982). Large body mass is a strong predictor of fighting performance in male–male contests (Andersson, 1994); however, other morphological, physiological and behavioral traits also influence competitive ability (e.g. Lailvaux and Irschick, 2006). House mice (Musmusculus Linnaeus) are an excellent model for studying the physical correlates of fighting performance in mammals because they possess a polygynous mating system where male mice acquire reproductive resources such as territory at least in part by fighting (Crowcroft, 1955; Hayashi, 1993), and highly competitive individuals have been shown to have greater reproductive success (De Fries and McClearn, 1970; Oakeshott, 1974; Kuse and De Fries, 1976; Dewsbury, 1982; Kaufman, 1983; Wolff, 1985; Hurst, 1987; Krackow, 1993; Meagher et al., 2000; Rolland et al., 2003). Interestingly, the relationship between body mass and fighting performance in male house mice does not adhere strictly to the ‘bigger is better’ paradigm. While some studies have found a direct correlation between body mass and competitive ability in male house mice (De Fries and McClearn, 1970; Oakeshott, 1974; Cunningham et al., 2013), others have reported no effect of body size (Benton et al., 1980; Rolland et al., 2003). More recent studies have suggested an optimal body mass for competitive ability in male house mice: Ruff et al. (2017) showed that fitness, estimated by the number of offspring produced, peaks at intermediate body sizes for male mice competing in semi-natural environments. Morris et al. (2017) found in the same experimental system that, although body mass did not differ significantly with territory-holding status, non-territory-holding mice exhibited greater variance in body size than mice that were able to consistently defend a territory. These results suggest that other aspects of the musculoskeletal system may be contributing to the unexplained variation observed in competitive ability. Previous morphological studies of male–male contests in vertebrates have focused overwhelmingly on the head, while the role of the postcranial musculoskeletal system has received much less attention. 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., 2003; Lassek and Gaulin, 2009; Morris et al., 2019; in macropodids: Jarman, 1983, 1989; Warburton 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 such comparisons of males with high and low competitive ability, postcranial measurements have been limited to limb segment lengths in lizards (López andReceived 30 August 2019; Accepted 3 January 2020 1School of Biological Sciences, University of Utah, Salt Lake City, UT 84112, USA. 2Department of Biosciences, Swansea University, Swansea SA2 8PP, UK. 3Department of Biology, Wofford College, Spartanburg, SC 29303, USA. *Author for correspondence (
[email protected]) A.N.C., 0000-0002-3195-9500 1 © 2020. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2020) 223, jeb213389. doi:10.1242/jeb.213389 Jo u rn al o f Ex p er im en ta lB io lo g y mailto:
[email protected] http://orcid.org/0000-0002-3195-9500 Martín, 2002; Huyghe et al., 2005; Kohlsdorf et al., 2006; Cameron et al., 2013). Here, we investigated whether highly competitive male house mice are more anatomically specialized for fighting performance than less competitive males. Our first aim was to test whether muscle mass was greater in competition-winning mice than in losers. We hypothesized that sexual selection would act most strongly on the muscle groups that are most important for fighting performance in male mice. Greater muscle mass is associated with (1) larger muscle cross-sectional area, which provides an increased capacity for force production, and/or (2) longer muscle fascicles, which allow for greater shortening velocity (Biewener, 2003). 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. Larger muscle forces require more robust bones to maintain appropriate safety factors (Alexander, 1981). Additionally, unpredictable loading directions during fighting select for a circular cross-sectional shape that makes limb bones more massive than those in animals specialized for running (Kemp et al., 2005). With respect to skeletal shape, we first predicted that winners would have relatively shorter and/or broader skulls to increase bite force by providing a greater mechanical advantage for the jaw adductors and more attachment area for the temporalis muscles, respectively (Biknevicius and Van Valkenburgh, 1996). Second, we expected winners to have broader cervical vertebrae to allow for larger cervical muscle attachment sites. Once the attacker has grasped an opponent with its jaws, larger neck muscles may facilitate jerking the head and pulling on the opponent with the teeth while resisting lateral loading of the attacker’s own head, which could lead to injury (Radinsky, 1981). The cervical vertebrae also serve as attachment sites for extrinsic appendicular muscles capable of protracting the forelimb (Evans, 1993), which may be useful during upright grappling. Our third prediction was that the scapulae of winners would havemore surface area for the attachment of muscles involved in transmitting force from the trunk to the forelimb (Carrier et al., 2006) and in stabilizing the shoulder joint. Finally, we expected anatomical mechanical advantage of the limbs to be greater in winners, allowing for increased force output against an opponent during grappling and/or pushing. MATERIALS AND METHODS Study population and experimental setup The present study measured musculoskeletal parameters in cadavers of mice that were subjects in a previous experiment, in which naive male house mice competed in a semi-natural environment for access to a single female housed within an optimal territory (Cunningham et al., 2013). In that experiment, male and female mice were sexually mature (≥4 months of age), and males were age matched with their competitors to control for interactions between age and competitive ability. All mice were procured from a population of wild-derived house mice maintained at the University of Utah, School of Biological Sciences. These animals were outbred descendants of a wild-caught population initially described by Meagher et al. (2000). Transparent acrylic semi-natural enclosures measuring 140×30×15 cm were constructed based on the semi-natural model system described in Carroll and Potts (2007). Taking advantage of the natural preference of mice for seclusion from conspecifics and predators (Wolff, 1985), an ‘optimal territory’ of 15×30×15 cm with opaque walls, nesting material, a single female and its own supply of food and water was placed at one end of the enclosure. The communal (non-optimal) area provided no opportunities for hiding and had shared food and water ad libitumwith no bedding materials, creating an incentive for competition. Competition assessment took place over the course of two rounds, with each round lasting 3 days. This duration was deemed appropriate for assessing competitive ability because mice quickly form social hierarchies via physical competition once introduced into a semi-natural environment (De Fries and McClearn, 1970; Hayashi, 1993). A group of four males and a single female participated in the first round. The second round of competition pitted three first-round winners against each other, and three losers against other losers. In all trials, both the population density and the operational sex ratio were much greater than those seen in self- regulating natural and semi-natural populations (Lidicker, 1976; Gomez et al., 2008).We expected that both the male-biased sex ratio and the relatively small size of the enclosures would help to identify individual differences in competitive ability, as larger enclosures may result in more chases in mice (Dewsbury, 1981, 1982).