Hemipenes in females of the mexican viviparous lizard Barisia imbricata (Squamata: Anguidae): an example of heterochrony in sexual development

Abstract

The sexual development of saurians follows a similar pattern to that described for other amniotes. Changes in the timing or sequence of development events are known as heterochrony. We describe the pattern of sexual development in the viviparous Mexican lizard Barisia imbricata and report heterochrony in the regression of hemipenes in this lizard. We collected gestating females; some lizards were subjected to partial hysterectomy and the embryos were processed using routine histological technique to assess gonadal development; the remaining embryos were used to assess the development of hemipenes. Other pregnant females were kept in captivity in individual terraria until the time of delivery. All neonates were sexed by eversion of hemipenes and some of their body characteristics were recorded. Several neonates were sacrificed and processed to establish gonadal histology and the young of the remaining litters were maintained in captivity to observe the fate of the hemipenes in both sexes. Gonadal development began at embryonic stage 33 and the hemipenes were visible at the same stage. In the neonates, the ovary contained oogonias and ovarian follicles, whereas the testicles showed testicular cords. All neonates had hemipenes and sex could only be established through direct observation of the reproductive ducts and gonadal histology. The hemipenes regression in the females begins after approximately 7 months of postnatal development and concludes at about 15 months of age. We think that the delayed regression of the hemipenes reflects evolutionary differences among reptiles and may be an indication of a stage in the evolutionary process of this species.

Embryonic development of a parthenogenetic vertebrate, the mourning gecko (Lepidodactylus lugubris)

“…In the lizard Anolis carolinensis and Anguis fragilis , paired phalluses develop in both sexes; however, hemipenes are large in males and hemiclitores are small in females . However, other lizards, such as Pogona vitticeps and Barisia imbricata , have female embryos with large, hemipenis‐like organs that are equal in size and shape with males, that subsequently regress prior to and just after hatching, respectively . Our results, coupled with results from the recent literature, make it clear that many aspects of squamate sexual development warrant more detailed examination.…”

“…64,81,82 However, other lizards, such as Pogona vitticeps and Barisia imbricata, have female embryos with large, hemipenis-like organs that are equal in size and shape with males, that subsequently regress prior to and just after hatching, respectively. 65,83 Our results, coupled with results from the recent literature, make it clear that many aspects of squamate sexual development warrant more detailed examination. Further investigation of external genital development in L. lugubris will be discussed in-detail separately.…”

Sex determination mode does not affect body or genital development of the central bearded dragon (Pogona vitticeps)

“…The extended retention of male traits in female P. vitticeps is interesting in an evolutionary context because female genitalia exhibit a far wider range of genital phenotypes than males, but these phenotypes are generally based on the default of a hemipenis form. Female genitalia in squamates vary from structures resembling rudimentary hemipenes to species where females have longer hemipenes and associated musculature than males [ 33 , 35 , 50 , 55 – 59 ]. In P. vitticeps , extended developmental hemipenis retention in females and male sex chromosome homogamety suggest that the ancestral programme of genital development may be biased towards hemipenis formation.…”

Development and differentiation of the reproductive system of Tropidurus catalanensis (Squamata: Tropiduridae)

“…The primordial follicles are organized at post‐hatching day 10 and the primary follicles possess polymorphic granulosa, on post‐hatching day 30 (Doddamani, ). In Barisia imbricata (Wiegmann, 1828) folliculogenesis begins at Stage 40 and there are follicles of different sizes at hatching (Martinez‐Torres, Rubio‐Morales, Piña‐Amado, & Luis, ). However, in the hatchlings of N. ocellatus (Neaves et al, ) and T. catalanensis , the cortex consists of several layers of proliferating oogonia.…”

“…Folliculogenesis is a key process for ovarian development and maturation, through which follicles are formed. In some species of lizards, the onset of folliculogenesis occurs at the latest stages of embryonic development (Martínez‐Torres et al, ; Miller, ), whereas in others is a post‐hatching event (Antonio‐Rubio et al, ; Doddamani, ; Neaves et al, ). Most studies of ovarian dynamics in lizards refer to the adult stage but little is known about the events that occur in the juvenile period, which is considered as a phase comparable to the stage of gonadal quiescence in adults (Ballinger & Nietfeldt, ; Ramírez Pinilla, ).…”