The evolution of female mole ovotestes evidences high plasticity of mammalian gonad development

Abstract

Previous studies of the reproductive biology and genetics of European moles (Talpa spp.) showed that all females of these species have ovotestes (gonads with testicular and ovarian tissue) instead of normal ovaries, a unique specialization among mammals. Females are fertile as their ovarian tissue is fully functional. Testicular tissue is abnormal and sterile, but produces high levels of testosterone. This phenomenon also characterizes other talpid species from Europe and North America. To study the origin of this singular reproductive specialization, we examined the gonads of several female specimens belonging to two critical taxa. Although large Japanese moles (Mogera wogura) posses ovotestes, greater Japanese shrew moles (Urotrichus talpoides) are characterized by normal ovaries. The results fit parsimoniously with a recent phylogenetic study that places Urotrichus relatively basal in the talpid tree and separate from the American shrew mole. Parsimony reconstruction on alternative phylogenetic hypotheses clearly indicates that reversal(s) must have occurred and suggests that a relatively simple genetic mechanism must be associated with the evolution of female hermaphroditism in moles.

Ovarian Organogenesis in Mammals: Mice Cannot Tell Us Everything

“…By contrast, it has been reported that some American mole species lack ovotestes, although they have a masculinised body including a penile clitoris, as described in moles with ovotestes [Rubenstein et al, 2003]. Similarly, not all Asian mole species have ovotestes [Carmona et al, 2008]. However, in most cases it is not known whether female moles without ovotestes are also territorial.…”

“…This suggests that the cause for the maintenance of regionalised ovaries in a particular species is probably not phylogenetic but adaptive. In the case of moles, Carmona et al [2008] have proposed that the testosterone produced by the testicular portion of the ovotestis during the non-breeding season could foment the aggressive behaviour of females, which have to defend their territories as males do. The mechanism by which testosterone induces aggressive behaviour, through the activation of the aromatase enzyme, which converts testosterone into estrogen in the brain, has been recently reported by Wu et al [2009].…”

“…This kind of XX ovotestes have been described in four European species of genus Talpa , T. europaea, T. occidentalis, T. romana, and T. stankovici [Popoff, 1911;Matthews, 1935;Jiménez et al, 1993;Sánchez et al, 1996], the desman Galemys pyrenaicus [Peyre, 1962], the star-nosed mole Condylura cristata [Mossman and Duke, 1973;Rubenstein et al, 2003], the American shrew mole Neurotrichus gibbsii [Rubenstein et al, 2003] and the large Japanese mole Mogera wogura [Carmona et al, 2008]. Barrionuevo et al [2004] reported a detailed morphological description of gonad development in the Iberian mole T. occidentalis, where XX gonads develop according to a testis-like pattern ( fig.…”

“…However, in most cases it is not known whether female moles without ovotestes are also territorial. In the case of Urotrichus talpoides , females lack ovotestes and are not territorial [Ishii, 1993;Carmona et al, 2008]. Carmona et al [2008], mapping the presence or absence of ovotestes in different phylogenies recently proposed for moles of the family Talpidae, showed that at least one reversal (appearance and further disappearance) must have occurred in the evolution of this trait, indicating a high plasticity in mammalian gonad development.…”

“…In the case of Urotrichus talpoides , females lack ovotestes and are not territorial [Ishii, 1993;Carmona et al, 2008]. Carmona et al [2008], mapping the presence or absence of ovotestes in different phylogenies recently proposed for moles of the family Talpidae, showed that at least one reversal (appearance and further disappearance) must have occurred in the evolution of this trait, indicating a high plasticity in mammalian gonad development. Such a developmental plasticity is necessary to explain how ovotestes may appear as a consequence of selective pressure in some species, but not in others of the same taxonomical group.…”