RESULTS AND DISCUSSION

X*Y females bit significantly harder than other females (Fig. 2; data are available on request from the corresponding author). They also bit harder than males, but not significantly so; bite force was similar between males and XX females. Table 2 shows the results of the Tukey's HSD test.

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Fig. 2.

Boxplot of bite forces of the three M. minutoides groups. Data are shown for males (n=19), XX females (n=18) and X*Y females (n=17). Limits of the boxes represent the upper and lower quartiles, the bar is the median, the whiskers represent the maximum and minimum value, or 1.5 times the interquartile distance in cases where outliers are present, and the circles are outliers. Asterisks indicate significant differences between means. Tukey's HSD test revealed a significant increase in bite force in X*Y females compared with XX females (P<0.01).

No major morphological differences appeared between the three groups,which overlapped in morphospace (Fig. 1C,D, Table 1).

X*Y females displayed a significantly greater centroid size than males and XX females (Table 2), even independently of age (Table 1). MANOVAs did not reveal any effect of the group on shape; however, they showed significant allometry shared by all groups (Table 1).

There was a significant size–bite force correlation (r≈0.6, d.f.=52, P<0.01 for both bones) when considering the data as a whole (i.e. not taking the groups into account). A relationship was also found between age and bite force (r=0.3, d.f.=49, P<0.05). In the linear model created, the type II ANOVA revealed that, once age and size were taken into account, bite force differences were no longer significant between the groups (F=1.28, d.f.=2, den. d.f.=42, P>0.2), although the tendency for X*Y females to have higher bite force than XX remained. In this model, age had no significant effect, and size remained the main explanatory variable.

We showed that in the African pygmy mouse, X*Y females bite harder than the XX females and, more surprisingly, also bite harder than males (although not significantly so). Limited shape variation between the sex chromosomal groups (Fig. 1C,D) shows that skull and mandible shape are not at the root of the higher bite force of X*Y females. It also suggests that the presence of the Y and/or X* chromosomes does not significantly influence shape. However, without considering the groups, we found a positive relationship between size and bite force, as shown in previous studies (Herrel et al., 2001; Lailvaux et al., 2004; Freeman and Lemen, 2008). Furthermore, X*Y females displayed a greater skull size, which appears to explain part of their increased bite force (Tables 1, 2). Performance changes independent of size but owing to behavioural differences between the groups are subtle and not significant, suggesting that aggressiveness has a much lower impact on performance variation than morphological determininants (here size).

Hormones are also known to influence performance, as demonstrated by hormonal and molecular screening of elite female athletes, which detected sex development disorders with hyperandrogenism (e.g. XY females) in an occurrence 200 times greater than in the general population (e.g. Fénichel et al., 2013). In our model, however, the M. minutoides X*Y females harbour typical ovarian anatomy (no ovotestes) and a normal anogenital distance, suggesting a low level of circulating androgen (Rahmoun et al., 2014), observations that have been recently confirmed by preliminary hormonal assays on testosterone (F.V., unpublished data). Therefore, the increased skull size of X*Y females appears to be the main cause of their higher bite force.

Although not much is known about the ecology of M. minutoides (Britton-Davidian et al., 2012), the advantages of having higher performance may be twofold. Higher bite force may increase the range of available food resources (Aguirre et al., 2003) by allowing the X*Y individuals to feed on harder food. Second, higher aggressiveness coupled with stronger bites may have a role in intra-sex competition: X*Y females may increase their reproductive success by taking dominance over other females via attacks (Lailvaux and Irschick, 2006). This has been shown for lizards, in which dominance, territorial defense and the outcome of fights are all linked to performance (Herrel et al., 2010; Lailvaux et al., 2004).

Chromosomal changes in the X*Y females may thus give them a dominant position, consistent with the hypothesis that an increase in fitness explains the maintenance of these females, despite the costly loss of the unviable YY embryos (Saunders et al., 2014). Considering our results and those of Saunders et al. (2014, 2016), it appears that the X*Y females obtain selective advantages through many aspects of their fitness: reproductive success, behaviour and whole-organism performance. The effect of the X* chromosome thus goes well beyond feminization, and is at the origin of a complex and multi-factorial X* syndrome that extends to life history traits, behaviour (Saunders et al., 2014, 2016), size variation and performance (present study). Interestingly, these X*Y females were characterized as ‘super females’ because they were shown to have a better reproductive output than the XX females (Saunders et al., 2014), but in addition, they present hyper-masculinized traits with an enhanced aggressiveness, larger skulls and stronger bite forces than males. It is notoriously hard to assign performance modifications to naturally occurring genetic changes, but this model offers a fantastic framework with which to further connect performance, morphology, behaviour and sex chromosomes.