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Keywords:

  • Mammals;
  • Descent of testes;
  • Mode of locomotion (gallop);
  • Specializations of testicular blood vessels;
  • Evolutionary compromise.

Abstract

On the cause of the mammalian descent of the testes (Descensus testiculorum)

Two explanations have been offered for the descent of the testes in mammals, both of which are frequently cited in the literature. Moore and co-workers argued that the phylogenetic rise of body temperature caused the translocation of the testes. According to Portmann, the descent of the testes was due to the evolution of the scrotum as a signal. However, both the sensibility of the extra-abdominal testes to temperature elevations and the optical effects of the scrotum can be interpreted as a consequence of testicular descent rather than as its cause.

The hypothesis presented in this paper suggests a new adaptive explanation for the descent of the testes in mammals and regards its development as an example of evolutionary compromise. Obvious disadvantages such as reduced protection of the extra-abdominal testes, “perforation” of the inguinal abdominal wall, and an increased loss of heat from the body core have to be outbalanced by a strong selective advantage. This advantage is seen in the development of a completely new, fast mode of locomotion - the gallop. The strong flexions and extensions of the vertebral column during gallop should cause intense fluctuations of intra-abdominal pressure. Fluctuations of intra-abdominal pressure severely impede continuous flow of blood in the abdominal veins. Periodically reduced venous drainage resulting in fluctuations of intra-testicular pressure would impair the process of spermiohistogenesis, which is dependent on an absolutely constant pressure within the testis. Thus, it is the displacement of the pressure sensitive testes out of the abdominal cavity that allows for the evolution of a fast mode of locomotion accompanied by strong fluctuations of intraabdominal pressure.

In the course of the phylogenetic translocation of the testes increasing specializations of the testicular blood vessels occur. In mammals possessing a scrotum the return flow of venous blood from the extra-abdominal testes to the abdominal cavity is supported by utilizing the energy of the arterial pulse (‘peripheral arterial pump’).

A model for the successive stages of the descent of the testes is illustrated in Figures 7–10. The morphological changes related to the phylogenetic descent of the testes, such as the specialization of the testicular blood vessels, the forming of a cremasteric sack in the inguinal region, and the differentiation of the inguinal or perineal integument into a scrotum can all be interpreted as serving one purpose: they aid in maintaining a constant intra-testicular pressure in spite of increasing fluctuations of intra-abdominal pressure and venous blood flow during the evolution of the gallop.

Although the blood vessels of the spermatic chord basically serve the same functions, they show markedly different specializations in Marsupials and Eutherians. This indicates that the descent of the testes has occurred independently, at least, in these two groups.

The explanation put forward here postulates a causal relationship between the mode of locomotion and the position of the testes. Mammals possessing testes wnich reside permanently within the abdominal cavity (‘Testiconda’) cannot gallop, whereas mammals with the ability to gallop must have (periodical or permanent) extraabdominal testes (‘Testiphaena’).