Sex reversal induces size and performance differences among females of the African pygmy mouse, Mus minutoides

Abstract

Differences in biological performance, at both intra- and inter-specific levels, have often been linked to morphology but seldom to behavioural or genotypic effects. We tested performance at the intraspecific level by measuring bite force in the African pygmy mouse, Mus minutoides. This species displays an unusual sex determination system, with sex-reversed, X*Y females carrying a feminizing X* chromosome. X*Y females cannot be differentiated from XX females based on external or gonadal morphology; however, they are known to be more aggressive. We found that bite force was higher in X*Y females than in other females and males. We then performed geometric morphometric analyses on their skulls and mandibles and found that the higher performance of X*Y females was mainly explained by a greater overall skull size. The effects of the X* chromosome thus go beyond feminization, and extend to whole-organism performance and morphology. Our results also suggest limited effects of behaviour on bite force.

Reproductive phenotype predicts adult bite‐force performance in sex‐reversed dragons (Pogona vitticeps)

“…The only other study of intraspecific bite‐force performance in a species with sex reversal was conducted on adults of the African pygmy mouse ( Mus minutoides ; Ginot et al, 2017). In contrast to the situation in P. vitticeps , sex‐reversed female mice (X*Y) were found to have greater bite‐force performance than both concordant females and males (Ginot et al, 2017).…”

“…The only other study of intraspecific bite‐force performance in a species with sex reversal was conducted on adults of the African pygmy mouse ( Mus minutoides ; Ginot et al, 2017). In contrast to the situation in P. vitticeps , sex‐reversed female mice (X*Y) were found to have greater bite‐force performance than both concordant females and males (Ginot et al, 2017). However, as in P. vitticeps , the greater bite force is associated with greater head size, thus highlighting the close relationship between head size and bite force (related to jaw muscle physiological cross‐sectional area, e.g., Erickson et al, 2003; Gans, 1982; Gröning et al, 2013; Santana et al, 2010; Sellers et al, 2017).…”

“…The accumulating evidence of species that employ both primary cues (genes and environment) to determine sex (transitional systems; Hill, Burridge, Ezaz, & Wapstra, 2018; Holleley et al, 2015; Holleley, Sarre, O'Meally, & Georges, 2016; Radder, Quinn, Georges, Sarre, & Shine, 2008; Shine, Elphick, & Donnellan, 2002), points to the existence of a continuum of states from complete genetic control via sex chromosomes to complete dependence on environmental influence over sex (Sarre, Georges, & Quinn, 2004). The potential for naturally occurring sex reversal (Baroiller & D'Cotta, 2016; Ginot, Claude, Perez, & Veyrunes, 2017; Holleley et al, 2015; Jiménez, Burgos, Caballero, & De La Guardia, 1988) is the hallmark of transitional systems. A small number of studies of terrestrial vertebrates indicate that the de‐coupling of chromosomal and phenotypic sex, via sex reversal, can result in individuals bearing a mixture of male‐like, female‐like, or novel traits (Deveson et al, 2017; Ginot et al, 2017; Li, Holleley, Elphick, Georges, & Shine, 2016).…”

Morphometric models for estimating bite force in Mus and Rattus: mandible shape and size do better than lever-arm ratios

“…Yet, bite force is also clearly under the influence of multiple factors intraspecifically, so that morphological variation may only partly explain performance variation. Among such factors, sex (Ginot et al, 2017), age (which was mostly uncontrolled in our wild species sample), behavior (notably motivational state), hormones, social status, health status, inbreeding or genetics, as well as a general plasticity of in vivo bite force depending on abiotic environmental conditions (e.g. temperature, food availability), might play an important role.…”

X inactivation in a mammal species with three sex chromosomes

“…Like in the wood lemming, females are XX, XX*, or X*Y, while all males are XY (Veyrunes et al 2010). Some life history and behavioural traits vary along with sex chromosome complement in M. minutoides, and interestingly, XX* females are much more similar to XX females than X*Y ones (Saunders et al 2014(Saunders et al , 2016Ginot et al 2017). This pattern is at least partly under the direct influence of genes on the sex chromosomes, but considering the paucity of genes on the Y chromosome and that most of them are specialized in male reproduction (Marshall Graves 2006), other mechanisms might be involved, such as a preferential X* inactivation in XX* females (Saunders et al 2014).…”