Adaptive plasticity of mammalian sperm production in response to social experience

Sperm competition theory predicts that males should invest prudently in ejaculates according to levels of female promiscuity. Males may therefore be sensitive to cues in their social environment associated with sexual competition, and tailor investment in sperm production accordingly. We tested this idea experimentally for the first time, to our knowledge, in a mammal by comparing reproductive traits of male house mice (Mus musculus domesticus) that had experienced contrasting encounter regimes with potential sexual competitors. We found that daily sperm production and numbers of sperm in the caput epididymis were significantly higher in subjects that had experienced a high encounter rate of social cues from three other males compared to those that had experienced a low encounter rate of social cues from just one other male. Epididymal sperm counts were negatively correlated with the frequency of scent-marking behaviour across all males in our study, suggesting that investment in ejaculate production may be traded off against traits that function in gaining copulations, although there was no difference in overall levels of scent marking between treatment groups. We conclude that social experience-mediated phenotypic plasticity in mammalian spermatogenesis is likely to be adaptive under sperm competition, enabling males to balance the energetic costs and paternity-enhancing benefits of ejaculate production, and is a potentially widespread explanation for intraspecific variation in ejaculate expenditure.