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Keywords:

  • African mole-rat;
  • Bathyergidae;
  • Fukomys;
  • Cryptomys;
  • spontaneous ovulation;
  • progesterone;
  • induced ovulation;
  • ovarian cyclicity;
  • penile ornamentation

Abstract

The giant mole-rat Fukomys mechowii is a cooperatively breeding, subterranean rodent inhabiting the Miombo woodland and savanna of south-central Africa, with reproduction occurring throughout the year. Across species within the family Bathyergidae, ovulation can be either induced by mating or spontaneous and the particular mechanism may correlate with patterns of seasonality, dispersal and opportunities for mating. We investigate the control of ovulation in F. mechowii, a species closely related to a spontaneously ovulating species but found in a habitat more typical of mole-rats with induced ovulation. Six wild-caught, non-reproductive females were removed from their natal colonies and non-invasively monitored for ovarian cyclicity by measuring urinary progesterone every 2 days, over 217 days. All six females had elevated progesterone profiles indicative of the luteal phase of the ovarian cycle, whether singly housed, separated from a male by a mesh screen (i.e. non-physical contact), or paired with a vasectomised male (full physical contact), although progesterone concentrations were significantly enhanced in the latter condition. Together with observations that male penile morphology is similar to other spontaneously ovulating bathyergids, these results strongly suggest that while ovarian cyclicity may occur spontaneously in F. mechowii, the presence of a male may have an additional stimulatory effect on ovulation. Comparative phylogenetic analysis revealed a positive correlation between seasonality in breeding and induced ovulation. Furthermore, a likelihood-based reconstruction suggests that induced ovulation is the ancestral state for the Bathyergidae and that this trait has been convergently lost in at least two lineages, giving rise to a spontaneous mode of ovulation.