The

epididymis The epididymis (; plural: epididymides or ) is a tube that connects a testicle to a vas deferens in the male reproductive system. It is a single, narrow, tightly-coiled tube in adult humans, in length. It serves as an interconnection between the ...

, which is a tube that connects a testicle to a vas deferens in the male reproductive system, evolved by retention of the mesonephric duct during regression and replacement of the mesonephros with the metanephric kidney. Similarly, during embryological involution of the paired mesonephric kidneys, each mesonephric duct is retained to become the epididymis, vas deferens, seminal vesicle and

ejaculatory duct The ejaculatory ducts (''ductus ejaculatorii'') are paired structures in male anatomy. Each ejaculatory duct is formed by the union of the vas deferens with the duct of the seminal vesicle. They pass through the prostate, and open into the ureth ...

(Wolffian duct). In reptiles and birds both the testes and excurrent ducts (efferent ducts, epididymis, vas deferens) occur in an intra-abdominal location ( testicond). Primitive mammals, such as the

monotreme Monotremes () are prototherian mammals of the order Monotremata. They are one of the three groups of living mammals, along with placentals (Eutheria), and marsupials (Metatheria). Monotremes are typified by structural differences in their brain ...

s (prototheria), also are testicond. Marsupial (metatheria) and placental ( eutheria) mammals exhibit differing degrees of testicular descent into an extra-abdominal scrotum.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. In scrotal mammals the epididymis is attached to the testes in an extra-abdominal position where the cauda epididymis extends beyond the lowest extremity of the testis. Hence, the cauda epididymis is exposed to the coolest of temperatures compared to all other reproductive structures. Whereas testicond reptiles contain an excurrent duct system, they lack male reproductive glands (absent seminal vesicles, prostate,

bulbourethral gland The bulbourethral glands or Cowper's glands (named for English anatomist William Cowper) are two small exocrine glands in the reproductive system of many male mammals (of all domesticated animals, they are absent only in dogs). They are homolog ...

s). Monotreme mammals are also testicond (like reptiles) and contain some, but not all (absent seminal vesicles) of the male reproductive glands observed in most metatherian and eutherian mammals. This combination of reptilian and mammalian structures within the monotreme reproductive tract has informed the evolution of the male reproductive tract in mammals. For example, the intra-abdominal low sperm storage capacity of the echidna (Tachyglossus aculeatus) epididymisDjakiew, D. & Jones R.C. (1981)
Structural differentiation of the male genital ducts of the echidna (Tachyglossus aculeatus)
Journal of Anatomy 132: 187-202. informed the role of the epididymis as the prime mover in the

evolution of descended testes in mammals 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 ...

as it relates to lower extra-gonadal temperatures enhancing epididymal sperm storage in scrotal mammals.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. Furthermore, the structure of the monotreme reproductive tract also informed prostate evolution in monotreme mammals.

Structural differentiation of the epididymis in reptiles

Drawing of epididymis of reptile, monotreme and scrotal mammals

The reptilian testis and epididymis typically undergo seasonal recrudescence coupled to the breeding season. All reptiles retain their testes and excurrent ducts within the abdomen (testicond). Generally, the reptilian epididymis does not exhibit the same degree of anatomical regionalizationAkbarsha, M.A., Kadalmani, B. &Tamilarasan, V. (2006)
Histological variation along and ultrastructural organization of the epithelium of the ductus epididymidis of the fan‐throated lizard Sitana ponticeriana Cuvier
Acta Zoologica 87: 181-196. compared to scrotal mammals (Figure 1). Indeed, the anatomical appearance of the epididymis of many reptilesRheubert, J.L., Sever, D.M., Siegel, D.S. & Trauth, S.E. (2015)
Male Reproductive Anatomy: The Gonadoducts, sexual segment of the kidney, and cloaca
Chapter 9. In: Rheubert, J. L., Siegel, D. S. and Trauth, S. E. (eds), Reproductive Biology and Phylogeny of Lizards. CRC Press, Boca Raton, FL. appears much more similar to the epididymis of monotremes than scrotal mammals (Figure 1). Anatomically, the gross morphologic features of the reptilian epididymis can vary between species, with some species of reptiles exhibiting just two anatomical regionsGist, D.H. (2011)
Hormones and the sex ducts and sex accessory structures of reptiles
Hormones and Reproduction of Vertebrates. Volume 3: Reptiles. Editors D.O. Norris and K.H. Lopez. Academic press. whereas others (snakes) may exhibit no observable regionalization of the epididymis.Sever, D.M. & Freeborn, L.R. (2012)
Observations on the anterior testicular ducts in snakes with emphasis on sea snakes and ultrastructure in the yellow-bellied sea snake, Pelamis platurus
Journal of Morphology 273: 324-336. A reptilian histologic initial segment of the epididymis has been extensively documented in several speciesHaider, S. & Rai, U. (1987)
Epididymis of the Indian wall lizard (Hemidactylus flaviviridis) during the sexual cycle and in response to mammalian pituitary gonadotrophins and testosterone
Journal of Morphology 191: 151-160.Van Wyk, J.H. (1995)
The male reproductive cycle of the lizard, cordylus giganteus (Sauria Cordylidae)
Journal of Herpetology 29: 522-535. homologous to the initial segment of mammals.Benoit, J. (1926). Recherches anatomiques, cytologiques et histophysiologiques sur et voies excretrices du testicule, cez les mammiferes. Archiv d’anatomie, d’histologie et d’embryologie 5: 173-412. The initial segment of the epididymis, first described in the guinea pig epididymis, is a histologically distinct region of tall pseudostratified columnar epithelium that receives spermatozoa from the ductuli efferentes (Figure 1). The epididymis is the primary sperm storage organ in male reptiles. In all reptiles and mammals the sperm storage region of the epididymis can objectively be identified as that distal extremity of the epididymis that exhibits a widened diameter of duct which contains additional layers of circumferential smooth muscle capable of contraction during ejaculation in direct continuity with the vas deferens (Figure 1). This sperm storage region has been described as the anatomical cauda epididymis or the histologic terminal segment of the epididymis.Glover, T. & Nicander, L. (1971). Some aspects of the structure and function in the mammalian epididymis. Journal of Reproduction and Fertility (Supplement) 13: 39-50. The caudal region of the reptilian epididymis, where sperm are stored, is an anatomical extension that narrows into a conical shape before forming the vas deferens.Cabral, S.R.P., Zieri, R., Franco-Belussi, l., De Sousa Santos, L.R., Zago, C.E.S., Taboga, S.R. & De Oliveira, C. (2011)
Morphological changes of the epididymis and description of the excurrent ducts of Phrynops geoffroanus (Testudines: Chelidae) during the reproductive cycle
The Anatomical Record 294: 145-155. The coiled epididymal duct within the cauda epididymis does not appear to be particularly long, and so may be limited in its capacity to store sperm in comparison to scrotal mammals. Limited sperm storage in the reptilian epididymis may be circumvented by the ability of female reptiles to store viable spermatozoa within their reproductive tract for utilization months or years after insemination.Sever, D.M. & Hamlett, W.C. (2002)
Female sperm storage in reptiles
Journal of Experimental Zoology 292: 187–199. A competing reproductive strategy to long-term sperm storage that explains the production of offspring after prolonged periods in the absence of males is facultative parthenogenesis.Booth, W. & Schuett, G.W. (2011)
Molecular genetic evidence for alternative reproductive strategies in North American pitvipers (Serpentes: Viperidae): long-term sperm storage and facultative parthenogenesis
Biological Journal of the Linnean Society104: 943-942. In either case, these female reproductive strategies may have evolved to counter limited sperm storage in the reptilian male epididymis.

Structural differentiation of the epididymis in monotreme mammals

The monotremes (short beaked echidna, long beaked echidna, platypus) are testicond seasonal breeding mammals that exhibit some characteristics of the reproductive tract found in reptiles (e.g. testicond, presence of a cloaca).Griffiths, M. (1978)
The Biology of the Monotremes.
Academic Press. The fully developed monotreme epididymis exhibits two anatomical regions, similar to some reptiles. The two anatomical regions of the monotreme epididymis closely correspond to just two histologic regions (Figure 1B), an initial segment and a terminal segment. Structural differentiation of the epididymis into just an initial segment and terminal segment, with no intervening middle segment, has also subsequently been observed as far back as the epididymis of sharks.Jones, N. & Jones, R.C. (1982). The structure of the male genital ducts of the Port Jackson shark, Heterodontus portusjacksoni, with particular reference to the genital ducts. Australian Journal of Zoology 30: 523-541.Jones, N., Jones, R.C. & Djakiew, D. (1984)
Luminal composition and maturation of spermatozoa in the male genital ducts of the Port Jackson shark, Heterodontus portusjacksoni
The Journal of Experimental Zoology 230: 417-426. In the monotreme echidna, the initial segment, where sperm undergo maturation, is much larger than the terminal segment (Figure 1B), the later segment being the sperm storage region of the epididymis.Djakiew, D. & Jones, J.C. (1983)
Sperm maturation, fluid transport, and secretion and absorption of protein in the epididymis of the echidna, Tachglossua aculeatus
Journal of Reproduction and Fertility 68: 445-456. In the monotreme echidna, the proportion (26% of total) of mature sperm stored intra-abdominally in the terminal segment of the epididymis is considerably less than the proportion of mature sperm stored in the epididymis of many eutherian mammals (50-75% of total) with descended testes.Dott, H.M. & Skinner, J.D. (1967)
A reassessment of extra-gonadal spermatozoa reserves in Suffolk rams.
Journal of Agricultural Sciences 69: 293-295.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.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. Hence, both reptiles and the monotreme echidna appear to have relatively limited sperm storage capacity in the testicond epididymis compared to mammals with the epididymis located in an extra-abdominal scrotum. This reduced sperm storage capacity of the monotreme testicond epididymis is further supported by observations that the sperm storage region of the epididymis of a testicond mammal (echidna) and a scrotal mammal (rat) are respectively 4% and 8% of the total length of the duct.Djakiew, D. & Jones , R.C. (1982)
Stereological analysis of the epididymis of the echidna (Tachyglossus aculeatus) and wistar rat.
Australian Journal of Zoology 30: 865-875. Significantly, the low intra-abdominal sperm storage capacity of the echidna epididymis helped inform the role of the epididymis as a prime mover in the

whereby lower extra-gonadal temperatures within the scrotal cauda epididymis reduces oxidative respiration of sperm, which enhances oxygen availability, thereby allowing greater epididymal sperm storage in the cooler scrotum of mammals.

Structural differentiation of the epididymis in marsupials and placental mammals

Most species of marsupial (metatherian) and placental (eutherian) mammals have evolved extra-gonadal testes, although a limited number of these mammals remain testicond or exhibit differing degrees of testicular descent. As a result of the epididymis being attached to the testis, and the cauda epididymis extending below the lower extremity of the testis (Figure 1C), it was proposed that the epididymis was the prime mover in the evolution of testicular decent, whereby the cauda epididymis preceded the testis into a scrotal location. The epididymis of marsupials (metatherians) and placental mammals (eutherians) has undergone further structural differentiation compared to that observed in prototherian mammals (Figure 1). In scrotal mammals, an initial segment is nearly always observed, however, additional histologically distinct regions have developed between the initial segment and the distal sperm storage region (terminal segment). These intervening histologic regions have been referred to as the middle segment. The histologic regions of the middle segment (Figure 1C) can vary in number in metatherianOrsi, M.A., Ferreira, A.L., de Melo, V.R. & Oliveira, M.C. (1981)
Regional histology of the epididymis in the South American opossum. Light microscopic study.
Anatomischer Anzeiger 150: 521-528.Cummins, J.M., Temple-Smith, P.D. & Renfree, M.B. (1986)
Reproduction in the male honey possum (Tarsipes rostratus: Marsupialia): the epididymis
American Journal of Anatomy 177(3): 385-401.Costa, S.F., Nogueira, J.C., Soares, B.A., Ambrosio, N.A., Chaves, A.S., Melo, L.Q. & Zangeronimo, M.G. (2015)
Morphology of scrotum and testicle, and spermatic pathways of Metachirus nudicaudatus (Geoffroy, 1803), Didelphidae-Marsupialia
Pesquisa Veterinaria Brasileira 35 (1): 69-83. and eutherianReid, B.L. & Cleland, K.W. (1957)
The structure and function of the epididymis I. The histology of the rat epididymis
Australian Journal of Zoology 5: 223-246.Nicander, L. & Glover, T. (1973)
Regional histology and fine structure of the epididymal duct in the golden hamster (Mesocricetus auratus)
Journal of Anatomy 114: 347-364. species of mammals. Beyond the histologic regions of the middle segment, the sperm storage region (anatomical cauda, histologic terminal segment) of scrotal mammals has enlarged to accommodate enhanced storage of sperm (Figure 1C). The storage of sperm in the scrotal epididymis is enhanced by cooler extra-abdominal temperatures. Indeed, experimental reflection of one epididymis into the warmer temperature of an abdominal location reduced sperm storage capacity by 75% compared to the contralateral epididymis that remained in the scrotum.Foldesy, R.G. & Bedford, J.M. (1982)
Biology of the scrotum. I. Temperature and androgen as determinants of the sperm storage capacity of the rat cauda epididymidis
Biology of Reproduction 26(4): 673-82. Significantly, cooler scrotal temperatures reduces oxidative respiration of sperm, thereby increasing oxygen availability to store more sperm per unit volume of duct, which has informed the

Trends in the evolution of the epididymis from testicond reptiles and monotremes to scrotal mammals

A histologically distinct initial segment of the epididymis is widely observed in many species of reptiles and even as far back as sharks. A large initial segment is also present in the epididymis of the testicond monotreme echidna. Furthermore, the scrotal epididymis of metatherian and eutherian mammals nearly all exhibit an initial segment which may contain histologically distinct sub-zones therein. Hence, the initial segment of the epididymis is well conserved in testicond vertebrates (reptiles, monotremes) and in scrotal metatherian and eutherian mammals (Figure 1). The status of the histologic middle segment of the epididymis in reptiles is incompletely defined (Figure 1A). Considering the wide variation in the anatomical structures of the four orders (Crocodilia, Sphenodontia, Squamata, Testudines) of reptilian epididymides and the paucity of histologic studies that correlate anatomical structure to histology, the evolution of the middle segment in reptiles, if present, remains to be delineated. In contrast, extensive studies of the echidna epididymis show that the monotreme epididymis lacks a middle segment. It is only in metatherian and eutherian mammals that a middle segment has been extensively documented. Whereas the initial segment of the epididymis often contains histologically distinct sub-zones therein, the downstream zones that collectively constitute the middle segment most likely evolved from the upstream sub-zones of the initial segment. The histologic terminal segment is the sperm storage region of the epididymis in reptiles, monotremes and both metatherian and eutherian mammals (Figure 1). The testicond epididymis (reptiles and monotremes) has a limited sperm storage capacity compared with the scrotal epididymis (metatherian and eutherian mammals), which has a much larger terminal segment to accommodate increased sperm storage. It is the cooler temperature of the scrotal epididymis that reduces oxidative respiration of sperm in the terminal segment, thereby increasing oxygen availability to store more sperm per unit volume of duct, thus informing the

. Whereas different and multiple histologic sub-regions may or may not occur within any segment of the epididymis, the histologic description of the epididymis consisting of an initial segment, middle segment and terminal segment provides a harmonized characterization that allows direct comparisons of homologous segments across species.

Summary and conclusion

The evolution of the epididymis from reptiles to mammals (Figure 1) entailed: # Retention of the histologic initial segment. # To varying degrees, elaboration of a histologic middle segment. # An increase in the length, volume and size of the histologic terminal segment of scrotal mammals, whereby the lower extra-abdominal (scrotal) temperature increased oxygen availability to sustain and store more sperm, thus providing a physiologic mechanism for the

References

{{reflist Evolution of tetrapods Scrotum