Journal of Biosciences

, Volume 35, Issue 1, pp 27–37

The evolutionary history of testicular externalization and the origin of the scrotum

Article

Abstract

This paper re-examines the evolution of the scrotum and testicular descent in the context of the recent phylogeny of mammals. The adaptive significance of testicular descent and scrotality is briefly discussed. We mapped four character states reflecting the position of testes and presence of scrotum onto recent mammalian phylogeny. Our results are interpreted as follows: as to the presence of testicondy in Monotremata and most of Atlantogenata, which represent the basal group of all eutherians, we argue that primary testicondy represents a plesiomorphic condition for Eutheria as well as for all mammals. This is in opposition to the previous hypothesis of Werdelin and Nilsonne that the scrotum may have evolved before the origin of mammals and then repeatedly disappeared in many groups including monotremes. We suggest that the scrotum evolved at least twice during the evolutionary history of mammals, within Marsupialia and Boreoeutheria, and has subsequently been lost by many groups; this trend is especially strong in Laurasiatheria. We suggest that the recent diversity in testicular position within mammals is the result of multiple selection pressures stemming from the need to provide conditions suitable for sperm development and storage, or to protect the male gonads from excessive physical and physiological disturbance.

Keywords

Evolution function mammals scrotum testicular descent 

Abbreviations used

AMH

anti-Mullerian hormone

CSL

cranial suspensory ligament

DA

descended ascrotal

DS

descended scrotal

INSL

insulin-like factor

M

marsupial

T

testicondy

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References

  1. Asher R J and Lehmann T 2008 Dental eruption in afrotherian mammals; BMC Biol. 6 14CrossRefPubMedGoogle Scholar
  2. Bedford J M 2004 Enigmas of mammalian gamete form and function; Biol. Rev. Camb. Philos. Soc. 79 429–460CrossRefPubMedGoogle Scholar
  3. Bedford J M 1978 Anatomical evidence for the epididymis as the prime mover in the evolution of the scrotum; Am. J. Anat. 152 483–507CrossRefPubMedGoogle Scholar
  4. Bilinska B, Kotula B M, Gancarczyk M, Sadowska J, Tabarowski Z, and Wojtusiak A 2003 Androgen aromatization in cryptorchid mouse testis; Acta Histochem. 105 57–65CrossRefPubMedGoogle Scholar
  5. Bininda-Emonds O R P, Cardillo M, Jones K E, MacPhee R D E, Beck R M D, Grenyer R, Price S A, and Vos R A et al. 2007 The delayed rise of present-day mammals; Nature (London) 446 507–512Google Scholar
  6. Burda H 2003 Adaptations for subterranean life; in Grzimek’s Animal life encyclopaedia, Vol 12 (Mammals I.) (New York: Gale Inc.) pp 69–78Google Scholar
  7. Carrick F, and Setchell B 1977 The evolution of the scrotum; in Reproduction and evolution (eds) J Calaby and T Tyndale-Biscoe (Canberra: Australian Academy of Science: Canberra) pp 165–170Google Scholar
  8. Chance M 1996 Reason for the externalization of the testis of mammals; J. Zool. London 239 691–695Google Scholar
  9. Coveney D, Shaw G, Hutson J M and Renfree M B 2002 The development of the gubernaculum and inguinal closure in the marsupial Macropus eugenii; J. Anat. 201 239–256CrossRefPubMedGoogle Scholar
  10. Einer-Jensen N and Hunter R 2005 Counter-current transfer in reproductive biology; Reproduction 129 9–18Google Scholar
  11. Freeman S 1990 The evolution of the scrotum: a new hypothesis; J. Theor. Biol. 145 429–445CrossRefPubMedGoogle Scholar
  12. Frey R 1991 Zur Ursache des Hodenabstiegs (Descensus testiculorum) bei Säugetieren; Z. Zool. Sys. Evolut-Forsch. 29 40–65Google Scholar
  13. Gallup G G Jr, Finn M M and Sammis B 2009 On the origin of descended scrotal testicles: the activation hypothesis; Evol. Psychol. 7 517–526Google Scholar
  14. Gilbert S F and Epel D 2009 Ecological developmental biology. Integrating epigenetics, medicine and evolution (Sunderland: Sinauer Associates)Google Scholar
  15. Griffiths A L, Renfree M B, Shaw G, Watts L M and Hutson J M 1993 The tammar wallaby (Macropus eugenii) and the Sprague-Dawley rat: comparative anatomy and physiology of inguinoscrotal testicular descent; J. Anat. 183 441–450PubMedGoogle Scholar
  16. Huson D, Richter D, Rausch C, Dezulian T, Franz M and Rupp R 2007 Dendroscope: an interactive viewer for large phylogenetic trees; BMC Bioinformatics 8 460Google Scholar
  17. Hutson J M, Shaw G, O W S, Short R V and Renfree M B 1988 Müllerian inhibiting substance production and testicular migration and descent in the pouch young of a marsupial; Development 104 549–556Google Scholar
  18. Ivell R 2007 Lifestyle impact and the biology of the human scrotum; Reprod. Biol. Endocrinol. 5 15CrossRefPubMedGoogle Scholar
  19. Ivell R and Bathgate R A D 2006 Hypothesis: neohormone systems as exciting targets for drug development; Trends Endocrinol. Metab. 17 123CrossRefPubMedGoogle Scholar
  20. Ivell R and Hartung S 2003 The molecular basis of cryptorchidism; Mol. Hum. Reprod. 9 175–181CrossRefPubMedGoogle Scholar
  21. Kleisner K 2008 The semantic morphology of Adolf Portmann: a starting point for the biosemiotics of organic form?; Biosemiotics 1 207–219Google Scholar
  22. Koskimies P, Suvanto M, Nokkala E, Huhtaniemi I T, McLuskey A, Themmen A P, and Poutanen M 2003 Female mice carrying a ubiquitin promoter-Insl3 transgene have descended ovaries and inguinal hernias but normal fertility; Mol. Cell. Endocrinol. 206 159–166CrossRefPubMedGoogle Scholar
  23. Lorenzo-Figueras M and Merritt A M 2002 Effects of exercise on gastric volume and pH in the proximal portion of the stomach of horses; Am. J. Vet. Res. 63 1481–1487CrossRefPubMedGoogle Scholar
  24. Mickoleit G 2004 Phylogenetische Systematik der Wirbeltiere (München: Verlag Dr. Friedrich Pfeil)Google Scholar
  25. Moore K L 1926 The biology of the mammalian testis and scrotum; Q. Rev. Biol. 1 4–50CrossRefGoogle Scholar
  26. Nation T R, Balic A, Southwell B R, Newgreen D F, and Hutson J M 2009 The hormonal control of testicular descent; Pediatr. Endocrinol. Rev. 7 22–31PubMedGoogle Scholar
  27. Nevo E 1999 Mosaic evolution of subterranean mammals. Regression, progression and global convergence (Oxford: Oxford University Press)Google Scholar
  28. Nightingale S S, Western P, and Hutson J M. 2008 The migrating gubernaculum grows like a limb bud; J. Pediatr. Surg. 43 387–390CrossRefPubMedGoogle Scholar
  29. Nikolaev S, Montoya-Burgos J I, Margulies E H, NISC Comparative Sequencing Program, Rougemont J, Nyffeler B and Antonarakis S E 2007 Early history of mammals is elucidated with the ENCODE multiple species sequencing data; PLoS Genet. 3 e2CrossRefPubMedGoogle Scholar
  30. Ottow B 1955 Biologische Anatomie der Genitalorgane und der Fortpflanzung der Säugertiere (Jena: Fischer)Google Scholar
  31. Pera I, Ivell R and Kirchhoff C 1996 Body temperature (37°C) specifically down-regulates the mRNA for the major sperm surface antigen CD52 in epididymal cell culture; Endocrinology 137 4451–4459CrossRefPubMedGoogle Scholar
  32. Portmann A 1952 Animal forms and patterns (London: Faber and Faber)Google Scholar
  33. Prasad A, Allard M and Green E 2008 Confirming the phylogeny of mammals by use of large comparative sequence data sets; Mol. Biol. Evol. 25 1795–1808CrossRefPubMedGoogle Scholar
  34. Rommel S A, Early G A, Matassa K A, Pabst D A and McLellan W A 1995 Venous structures associated with thermoregulation of phocid seal reproductive organs; Anat. Rec. 243 390–402CrossRefPubMedGoogle Scholar
  35. Ruibal R 1957 The evolution of the scrotum; Evolution 11 376–378Google Scholar
  36. Seiffert E R 2007 A new estimate of afrotherian phylogeny based on simultaneous analysis of genomic, morphological, and fossil evidence; BMC Evol. Biol. 7 224CrossRefPubMedGoogle Scholar
  37. Setchell B 1978 The mammalian testis (London: Paul Elek)Google Scholar
  38. Setchell B 1998 The Parkes lecture: heat and the testis; J. Reprod. Fertil. 114 179–194PubMedCrossRefGoogle Scholar
  39. Shaw G, Renfree M and Short R 1990 Primary genetic control of sexual differentiation in marsupials; Aust. J. Zool. 37 443–450CrossRefGoogle Scholar
  40. Short R V 1997 The testis: the witness of the mating system, the site of mutation and the engine of desire; Acta. Paediatr. Suppl. 422 3–7PubMedGoogle Scholar
  41. Starck D 1995 Lehrbuch der speciellen Zoologie. Band II: Wirbeltiere. 5. Teil: Säugertiere (Jena: Gustav Fischer)Google Scholar
  42. Waters P D, Dobigny G, Waddell P J and Robinson T J 2007 Evolutionary history of LINE-1 in the major clades of placental mammals; PLoS ONE 2 e158CrossRefPubMedGoogle Scholar
  43. Werdelin L and Nilsonne A 1999 The evolution of the scrotum and testicular descent in mammals: a phylogenetic view; J. Theor. Biol. 196 61–72CrossRefPubMedGoogle Scholar
  44. Wildman D E, Uddin M, Opazo J C, Liu G, Lefort V, Guindon S, Gascuel O, Grossman L I et al. 2007 Genomics, biogeography, and the diversification of placental mammals; Proc. Natl. Acad. Sci. U SA 104 14395–14400CrossRefGoogle Scholar
  45. Williams M and Hutson J 1991 The phylogeny of testicular descent; Pediatr. Surg. Int. 6 162–166Google Scholar

Copyright information

© Indian Academy of Sciences 2010

Authors and Affiliations

  1. 1.Department of Philosophy and History of ScienceCharles UniversityPragueCzech Republic
  2. 2.School of Molecular and Biomedical ScienceUniversity of AdelaideAdelaideAustralia

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