The Italian Wall Lizard Podarcis siculus as a Biological Model for Research in Male Reproductive Toxicology

Abstract

Spermatogenesis is a genetically driven differentiation process that occurs in the testis and leads to the formation of spermatozoa. This process is extensively studied in several experimental models, particularly in vertebrates that share the morphological structure and functionality of the mammalian testis. Although reptiles are not generally considered biological models, the lizard Podarcis siculus has represented a suitable organism for the study of spermatogenesis over the years. In this lizard, the process of spermatogenesis is regulated by the interaction between systemic factors such as gonadotropins and local factors, i.e., molecules produced by the somatic and germinal cells of the testis. Many exogenous substances are able to alter the production of these regulative factors, thus altering the course of spermatogenesis, and P. siculus has proven to be an excellent model for studying the effects of various endogenous or exogenous substances on mechanisms underlying spermatogenesis. This review summarizes the available data on the effects of different substances on the control of spermatogenesis, highlighting the induced morphological and molecular alterations. Overall, the data show that sex hormone levels as well as the final stages of spermatogenesis are most affected by an imbalance of endogenous compounds or contamination by environmental pollutants. This is helpful for the male individual, since the damage, not affecting the spermatogonial stem cells, can be considered transient and not irreversible.

Keywords: endocrine disrupting compounds; environmental contaminants; reptiles; spermatogenesis; testis.

Figure 1

Male specimen of Podarcis siculus in an antrophic environment.

Figure 2

Cross-section of control lizard testis, stained with Mallory’s trichrome, during the two main phases of the reproductive cycle: reproductive period (A) and summer stasis (B). (A) During this period, the seminiferous tubules are characterized by a large lumen and a thick wall with germ cells in all stages of differentiation, i.e., spermatogonia (Spg), spermatocytes I (Spc I) and II (Spc II), spermatids (Spt), and spermatozoa (Spz). Triangular-shaped Sertoli cells (arrow) and Leydig cells in the interstitial space (asterisk) are clearly visible. (B) In this period, seminiferous tubules are smaller and characterized by the absence of lumen and the presence of only spermatogonia (Spg) in the thin wall. Sertoli cells (arrow) and Leydig cells in the interstitial space (asterisk) are always present. Scale bars at 10 µm.

Figure 3

Cross-section of lizard testis during reproductive period, stained with picrosirius red: testis of control animals (A) and testis of glyphosate-treated animals (B). (B) Gaps (rectangles) are evident in the testicular epithelium as well as fibrosis (arrow) on the outside of the tubules. Rosette-shaped cell aggregates (arrowhead). Scale bars at 20 µm.

Figure 4

Cross-section of the lizard testis during reproductive period, stained with eosin: testis of control animals (A) and testis of EDCs-treated animals (B). (A) the germinal epithelium is characterized by cells in all stages of differentiation as spermatogonia (Spg), spermatocytes I and II (Spc I and II), spermatids (Spt), and spermatozoa (Spz). (B) The germinal epithelium is characterized by cells in the early stages of differentiation as spermatogonia (Spg), spermatocytes I and II (Spc I and II). Both spermatids (Spt) and spermatozoa (Spz) are not evident in treated animals. Sertoli cells (arrow). Leydig cells (*). Scale bars at 20 µm.