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Evolution of descended testes in mammals

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Mammals are the only animals in which the testes descend from their point of origin into a scrotum. Concurrently, mammals are the only class of vertebrates to evolve a prostate gland starting with prostate evolution in monotreme mammals.

Testicular descent occurs to a variable degree in various mammals, ranging from virtually no change of position from the abdominal cavity (monotremes, elephants, and hyraxes); through migration to the caudal end of the abdominal cavity (armadillos, whales, and dolphins); migration just through the abdominal wall (hedgehogs, moles, seals); formation of a sub-anal swelling (pigs, rodents); to the development of pronounced scrota (primates, dogs, ruminants) in mammals.[1]

Since the descent of the testes into a scrotal pouch subjects the animal to enhanced risk of accidental damage and/or vulnerability from predators and rivals, presumably there must be some evolutionary adaptive advantage to testicular descent. It has been proposed that the scrotum may act as a form of sexual decoration.[2] A scrotal location also exposes the testes to a reduced temperature below that of the body,[3] which has been suggested to reduce the spontaneous rate of germ cell mutations.[4]

Mechanism for the sperm storage region of the epididymis promoting testicular descent

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An alternative proposal is that testicular descent was preceded, and possibly influenced, by migration of the sperm storage region of the epididymis to a cooler extra-abdominal location.[5][6][7] The evolutionary adaptive advantage of testicular descent into an extra-abdominal position may be related more to the enhanced sperm storage capacity of the epididymis at lower extra-abdominal temperatures than to the testis itself.[7] Greater sperm storage capacity in the epididymis has been associated with enhanced fertility. In this context, the proportion (26% of total) of mature sperm stored intra-abdominally in the monotreme epididymis[8] is considerably less than the proportion of mature sperm stored in the epididymis of many eutherian mammals (50-75% of total) with descended testes.[9][10][11] Moreover, this increase in scrotal storage of sperm corresponds with epididymis evolution from reptiles to mammals.

The mechanism by which sperm storage in the epididymis is enhanced at lower extra-abdominal temperatures has been shown to be a consequence of the biophysics of oxygen availability and sperm oxidative respiration.[12] The cauda epididymis, where sperm are stored, can be up to 7 °C below abdominal temperatures. For a reduction in temperature of 7 °C the respiration rate of sperm declines by one half, and the solubility of oxygen in solution increases by approximately 10%.[12] Hence for a reduction in temperature of 7 °C the availability of oxygen is doubled, and hence twice as many sperm can be stored per unit volume of epididymal duct.[12] This increased sperm reserve at lower extra-abdominal temperatures has been related to enhanced fertility which provides an evolutionary advantage to the survival of the species.[7]

In conclusion, the evolution of descended testes was promoted by the lower extra-abdominal temperature of the cauda epididymis which increased oxygen availability to sustain and store more sperm.[12]

References

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  1. ^ Setchell B.P. (1978). The Mammalian Testis. Cornell University Press, Ithaca, New York.
  2. ^ Portman, A. (1952). Animal Forms and Patterns, Faber & Faber, London.
  3. ^ Moore C.R. (1923). On the relationship of the germinal epithelium to the position of the testis. Anatomical Record 34: 337-358.
  4. ^ Ehrenberg L., von Ehrenstein G., Hedgram A. (1957). Gonad temperature and spontaneous mutation-rate in man. Nature 180: 1433-1434.
  5. ^ Heller, R.E. (1929). New evidence for the function of the scrotum. Physiology Zoology 2: 9-17.
  6. ^ Glover T.D. (1973). Aspects of sperm production in some East African mammals. Journal of Reproduction and Fertility 35: 45-53.
  7. ^ a b c Bedford H.M. (1978). Anatomical evidence for the epididymis as the prime mover in the evolution of the scrotum. American Journal of Anatomy 152: 483-508.
  8. ^ Djakiew D. & Jones J.C. (1981). Structural differentiation of the male genital ducts of the echidna (Tachyglossus aculeatus). Journal of Anatomy 132: 187-202.
  9. ^ Dott H.M. & Skinner J.D. (1967). A reassessment of extragonadal spermatozoa reserves in Suffolk rams. Journal of Agricultural Sciences 69: 293-295.
  10. ^ Orgebin-Crist M.C. (1968). Gonadal and epididymal sperm reserves in the rabbit; Estimation of the daily sperm production. Journal of Reproduction and Fertility 15: 15-25.
  11. ^ Amann R.P., Johnson L., Thompson D.L. & Pickett B.W. (1976). Daily spermatozoal production, epididymal spermatozoal reserves and transit time of spermatozoa through the epididymis of the rhesus monkey. Biology of Reproduction 15: 586-592.
  12. ^ a b c d Djakiew D. & Cardullo R. (1986). Lower temperature of the cauda epididymidis facilitates the storage of sperm by enhancing oxygen availability. Gamete Research 15: 237-245. Reprint available from the author.
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