Variation in ovarian morphology in four species of New World moles with a peniform clitoris

Abstract

Female moles of the Old World genus Talpa display a curious suite of reproductive features that include a peniform clitoris and ovaries with a discrete interstitial gland or testis-like region (so-called 'ovotestes'). The masculinization of the female external genitalia in Talpa has accordingly been linked with secretion of androgens from the interstitial gland region of the fetal gonad. Although their ovarian morphology has received less attention, some species of New World moles also have ovaries with a pronounced interstitial gland (for example star-nosed mole, Condylura cristata), whereas females of other species do not (for example eastern mole, Scalopus aquaticus). Although it is difficult to determine the sex of both Old and New World moles, published accounts describing the external genitalia of female moles are available only for Talpa. The hypothesis that masculinization of the female external genitalia in moles is associated with the presence of an ovarian interstitial gland (OIG) was tested in the present study by using a comparative approach to determine whether these features are ever found in isolation of one another. Three genera of North American moles (Scapanus, Condylura and Neurotrichus) were studied and a peniform clitoris was found in all three species, but OIG were found in only two of three genera. The ovaries of S. latimanus and S. orarius were unremarkable, with no evidence of a discrete interstitial gland or testis-like region. Mapping these results onto recent talpid phylogenies indicates that loss of the bipolar ovarian morphology is a derived trait in Scapanus, and conclusively demonstrates that masculinization of the external genitalia in female moles can develop in the presence or absence of 'ovotestes'.

Ovarian Organogenesis in Mammals: Mice Cannot Tell Us Everything

“…Jiménez, unpublished data]. 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].…”

“…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.…”

The spatio-temporal pattern of testis organogenesis in mammals - insights from the mole

“…Female moles represent the only case of generalized XX true hermaphroditism described so far in mammals, since all of them are fertile despite that they have bilateral ovotestes (gonads with both ovarian and testicular tissue) instead of normal ovaries (Jiménez et al, 1993;Sánchez et al, 1996, Rubenstein et al, 2003. Barrionuevo et al (2004a) studied the gonad development in the Iberian mole, Talpa occidentalis, showing that the testicular portion of the ovotestes in XX moles develops in a testis-like pattern.…”

Natural Exceptions to Normal Gonad Development in Mammals

“…The presence of ovotestes described in T. europaea [Matthews, 1935] and T. occidentalis [Jiménez et al, 1993] was also demonstrated in all other European species analysed and in some, but not all, North American [Rubenstein et al, 2003] and Asian [Carmona et al, 2008] talpid moles. With this information, subsequent authors have studied the evolutionary origin of this trait by performing a parsimony reconstruction of the presence/absence of ovotestes on alternative phylogenetic hypotheses on talpid mole evolution.…”

“…It is noteworthy that some juvenile females captured during the nonbreeding season and exhibiting the largest ovotestes had serum testosterone levels that were even higher than those of adult males captured during the same period. While the presence of circulating androgens may explain the partial development of Wolffian duct derivatives, such as the rudimentary epididymides mentioned above, it is not clear if the development of the peniform clitoris of female moles is also a consequence of the testosterone produced by their ovotestes [Rubenstein et al, 2003]. Both male and female gonads produce testosterone seasonally but follow an inverted periodicity: males exhibit higher levels during the breeding season, and females produce most testosterone during the non-breeding season [Jiménez et al, 1993;Whitworth et al, 1999].…”