Prostate evolution in monotreme mammals

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The monotremes (egg laying mammals) represent the order of extant mammals most distantly related to humans. The platypus (Ornithorhynchus anatinus) is indigenous to eastern Australia; the short-beaked echidna (Tachyglossus aculeatus) is indigenous to Australia and Papua New Guinea; whereas the long-beaked echidna (Zaglossus bruijni) is restricted to Papua New Guinea and Irian Jaya. [1] [2] Since monotremes exhibit characteristics common with both reptiles (e.g. presence of a cloaca) and therian mammals (e.g. mammary glands), they are of great interest for the study of mammalian evolution. [1] [2]

Contents

Monotremes exhibit a combination of reptilian and mammalian characteristics

Male monotremes are testicond (have intraabdominal testes) with the testes undergoing seasonal emergence during winter. The fully developed seminiferous tubules exhibit distinctly small stages of spermatogenesis in that more than one stage is often observed in a cross section of the tubule, [3] a characteristic of spermatogenesis that has also been observed in a reptile, [4] common in birds [5] [6] and man. [7]

The monotreme paired excurrent ducts (ductuli efferentes, epididymides [8] and vasa deferentia) empty into a single urethra. [2] Glandular tissue surrounds the urethra into which a pair of bulbourethral glands (Cowper's glands) empty at the base of the penis. The intraabdominal testes and excurrent ducts, along with the presence of a cloaca exhibit homology to the reptilian male reproductive tract. [1] [2]

The 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 intraabdominal low sperm storage capacity of the echidna epididymis [8] informed the role of the epididymis as a prime mover in the evolution of descended testes in mammals as it relates to lower extragonadal temperatures enhancing epididymal sperm storage in scrotal mammals. [9]

The glandular designation of periurethral tissue within the monotreme male reproductive tract has been a matter of scientific discussion for approximately two centuries. [10] [11] [12] [13] Examination of the monotreme periurethral tissue has been limited by the availability of these protected and relatively rare mammals, hence, the long time line for scientific research of reproductive tissue between studies.

Structure of the monotreme prostate

Figure 1. Aspermatogenic echidna prostate Figure 1. Aspermatogenic Echidna Prostate.jpg
Figure 1. Aspermatogenic echidna prostate
Figure 2. Spermatogenic echidna prostate Figure 2. Spermatogenic Echidna Prostate.jpg
Figure 2. Spermatogenic echidna prostate

The glandular tissue surrounding the monotreme urethra most likely represents a rudimentary prostate. [13] There are no periurethral glands in reptiles. Hence, the evolution of the prostate gland is unique to mammals. Primordial periurethral glands have been described in the platypus as secretory glandular tissue surrounding the length of the urethra. [12] The periurethral tissue exhibits regional swelling, being widest immediately beneath the bladder and progressively reducing in thickness along the length of the urethra. [12] Surrounding the periurethral glands is a urethral muscularis. [12] Observations in the platypus of the periurethral glands were non-committal as to homology with the prostate. [11] [12] Subsequently, the periurethral tissue in the echidna was definitively identified as a rudimentary prostate. [13] This is supported by:

  1. anatomically these glands are placed at their widest at the base of the bladder, [10] [11] which is similar in location for the prostate in other mammals,
  2. histologic lining of the echidna urethra with transitional epithelium (Figures 1 & 2), and not post-prostate urethral lining of pseudostratified or stratified columnar epithelium observed in eutherian mammals,
  3. location of periurethral glands with 9-11 buds per cross section surrounding and exiting into the urethra, [13]
  4. histology of simple columnar secretory cells lining compound alveolar glands, [12] [13]
  5. the glandular tissue is surrounded by a muscularis to facilitate expulsion of secretory products into the urethra, [12] [13]
  6. seasonal changes in echidna glandular development, [13] whereby in aspermatogenic animals the glandular tissue surrounding the urethra is less developed (Figure 1) than during the breeding season when the secretory glands surrounding the urethra of spermatogenic animals appear well developed (Figure 2) coinciding with elevated levels of testosterone and active spermatogenesis. [1] [2]

In aggregate, these characteristics of glandular tissue surrounding the urethra identify a rudimentary disseminate prostate in monotremes. [13]

Related Research Articles

<span class="mw-page-title-main">Prostate</span> Gland of the male reproductive system in most mammals

The prostate is both an accessory gland of the male reproductive system and a muscle-driven mechanical switch between urination and ejaculation. It is found in all male mammals. It differs between species anatomically, chemically, and physiologically. Anatomically, the prostate is found below the bladder, with the urethra passing through it. It is described in gross anatomy as consisting of lobes and in microanatomy by zone. It is surrounded by an elastic, fibromuscular capsule and contains glandular tissue, as well as connective tissue.

<span class="mw-page-title-main">Testicle</span> Internal organ in the male reproductive system

A testicle or testis is the male gonad in all bilaterians, including humans. It is homologous to the female ovary. The functions of the testicles are to produce both sperm and androgens, primarily testosterone. Testosterone release is controlled by the anterior pituitary luteinizing hormone, whereas sperm production is controlled both by the anterior pituitary follicle-stimulating hormone and gonadal testosterone.

<span class="mw-page-title-main">Echidna</span> Family of mammals

Echidnas, sometimes known as spiny anteaters, are quill-covered monotremes belonging to the family Tachyglossidae, living in Australia and New Guinea. The four extant species of echidnas and the platypus are the only living mammals that lay eggs and the only surviving members of the order Monotremata. The diet of some species consists of ants and termites, but they are not closely related to the American true anteaters or to hedgehogs. Their young are called puggles.

<span class="mw-page-title-main">Bulbourethral gland</span> Gland in males to help with sperm health

The bulbourethral glands or Cowper's glands are two small exocrine and accessory glands in the reproductive system of many male mammals. They are homologous to Bartholin's glands in females. The bulbourethral glands are responsible for producing a pre-ejaculate fluid called Cowper's fluid, which is secreted during sexual arousal, neutralizing the acidity of the urethra in preparation for the passage of sperm cells. The paired glands are found adjacent to the urethra just below the prostate, seen best by screening (medicine) MRI as a tool in preventative healthcare in males. Screening MRI may be performed when there is a positive prostate-specific antigen on basic laboratory tests. Prostate cancer is the second-most common cause of cancer-related mortality in males in the USA.

<span class="mw-page-title-main">Seminal vesicles</span> Pair of simple tubular glands posteroinferior to the urinary bladder of male mammals

The seminal vesicles are a pair of convoluted tubular accessory glands that lie behind the urinary bladder of male mammals. They secrete fluid that partly composes the semen.

<span class="mw-page-title-main">Epididymis</span> Tube that connects a testicle to a vas deferens

The epididymis is an elongated tubular structure attached to the posterior side of each one of the two male reproductive glands, the testicles. It is a single, narrow, tightly coiled tube in adult humans, 6 to 7 centimetres in length; uncoiled the tube would be approximately 6 m long. It connects the testicle to the vas deferens in the male reproductive system. The epididymis serves as an interconnection between the multiple efferent ducts at the rear of a testicle (proximally), and the vas deferens (distally). Its primary function is the storage, maturation and transport of sperm cells.

<span class="mw-page-title-main">Spermatogenesis</span> Production of sperm

Spermatogenesis is the process by which haploid spermatozoa develop from germ cells in the seminiferous tubules of the testicle. This process starts with the mitotic division of the stem cells located close to the basement membrane of the tubules. These cells are called spermatogonial stem cells. The mitotic division of these produces two types of cells. Type A cells replenish the stem cells, and type B cells differentiate into primary spermatocytes. The primary spermatocyte divides meiotically into two secondary spermatocytes; each secondary spermatocyte divides into two equal haploid spermatids by Meiosis II. The spermatids are transformed into spermatozoa (sperm) by the process of spermiogenesis. These develop into mature spermatozoa, also known as sperm cells. Thus, the primary spermatocyte gives rise to two cells, the secondary spermatocytes, and the two secondary spermatocytes by their subdivision produce four spermatozoa and four haploid cells.

<span class="mw-page-title-main">Cloaca</span> Posterior opening in zoology

A cloaca, pl.: cloacae, is the rear orifice that serves as the only opening for the digestive, reproductive, and urinary tracts of many vertebrate animals. All amphibians, reptiles, birds, and a few mammals, have this orifice, from which they excrete both urine and feces; this is in contrast to most placental mammals, which have two or three separate orifices for evacuation and reproduction. Excretory openings with analogous purpose in some invertebrates are also sometimes called cloacae. Mating through the cloaca is called cloacal copulation and cloacal kissing.

<span class="mw-page-title-main">Male reproductive system</span> Reproductive system of the human male

The male reproductive system consists of a number of sex organs that play a role in the process of human reproduction. These organs are located on the outside of the body, and within the pelvis.

<span class="mw-page-title-main">Short-beaked echidna</span> Spiny furred egg-laying mammal from Australia

The short-beaked echidna, also known as the short-nosed echidna, is one of four living species of echidna and the only member of the genus Tachyglossus.

<span class="mw-page-title-main">Human reproductive system</span> Organs involved in reproduction

The human reproductive system includes the male reproductive system which functions to produce and deposit sperm; and the female reproductive system which functions to produce egg cells, and to protect and nourish the fetus until birth. Humans have a high level of sexual differentiation. In addition to differences in nearly every reproductive organ, there are numerous differences in typical secondary sex characteristics.

<span class="mw-page-title-main">Spermiogenesis</span> Final stage of spermatogenesis, involving spermatid maturation

Spermiogenesis is the final stage of spermatogenesis, during which the spermatids develop into mature spermatozoa. At the beginning of the stage, the spermatid is a more or less circular cell containing a nucleus, Golgi apparatus, centriole and mitochondria; by the end of the process, it has radically transformed into an elongated spermatozoon, complete with a head, midpiece, and tail.

The development of the reproductive system is the part of embryonic growth that results in the sex organs and contributes to sexual differentiation. Due to its large overlap with development of the urinary system, the two systems are typically described together as the genitourinary system.

<span class="mw-page-title-main">Monotreme</span> Order of egg-laying mammals

Monotremes are mammals of the order Monotremata. They are the only known group of living mammals that lay eggs, rather than bearing live young. The extant monotreme species are the platypus and the four species of echidnas. Monotremes are typified by structural differences in their brains, jaws, digestive tract, reproductive tract, and other body parts, compared to the more common mammalian types. Although they are different from almost all mammals in that they lay eggs, like all mammals, the female monotremes nurse their young with milk.

<span class="mw-page-title-main">Male accessory gland</span> Sexual gland in males

Male accessory glands (MAG) in humans are the seminal vesicles, prostate gland, and the bulbourethral glands. In insects, male accessory glands produce products that mix with the sperm to protect and preserve them, including seminal fluid proteins. Some insecticides can induce an increase in the protein content of the male accessory glands of certain types of insects. This has the unintended effect of increasing the number of offspring they produce.

<span class="mw-page-title-main">Male accessory gland infection</span> Medical condition

Male accessory gland infection (MAGI) is a condition with signs of inflammation involving one or more sites in the male genital tract. Diagnosis is made according to parameters defined by the World Health Organization, and it is particularly made in relation to infectious or inflammatory causes of male infertility.

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.

The epididymis, 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. In reptiles and birds both the testes and excurrent ducts occur in an intra-abdominal location (testicond). Primitive mammals, such as the monotremes (prototheria), also are testicond. Marsupial (metatheria) and placental (eutheria) mammals exhibit differing degrees of testicular descent into an extra-abdominal scrotum. 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.

<span class="mw-page-title-main">Daniel Djakiew</span> Australian academic

Daniel Djakiew is a scholar, researcher, teacher, and tenured full professor in the Department of Biochemistry and Molecular & Cellular Biology, School of Medicine, Georgetown University, Washington DC.

References

  1. 1 2 3 4 Griffiths, M. (1968). Echidnas. Pergamon Press.
  2. 1 2 3 4 5 Griffiths, M. (1978). The Biology of the Monotremes. Academic Press.
  3. ↑ Djakiew, D. (1984). Reproduction in the Male Echidna (Tachyglossus aculeatus) with Particular Emphasis on the Epididymis. Ph.D. Thesis, University of Newcastle, Australia.
  4. ↑ Sousa, A.L. Campos-Junior, P.H.A., Costa, G.M.J. and de Franca, L.R. (2014). Spermatogenic cycle length and sperm production the freshwater turtle Kinosternon scorpioides. Biology of Reproduction, 90; 1-10.
  5. ↑ Aire, T.A., Olowo-okorun, M.O. , Ayeni, J.S. (1980). The seminiferous epithelium of the Guinea fowl (Numida meleagris). Cell and Tissue Research, 205; 319-325.
  6. ↑ Abdul-Rahman, I.I., Obese, F.Y., Robinson, J.E. (2017). Spermatogenesis and cellular associations in the seminiferous epithelium of Guinea cock (Numida meleagris). Canadian Journal of Animal Science, 97; 241-249.
  7. ↑ Clermont Y. (1963). The cycle of the seminiferous epithelium in man. American Journal of Anatomy, 112; 35-51.
  8. 1 2 Djakiew, D. and Jones, R. (1981). Structural differentiation of the male genital ducts of the echidna (Tachyglossus aculeatus). Journal of Anatomy; 132; 187-202.
  9. ↑ Djakiew, D. and Cardullo, R. (1986). Lower temperature of the cauda epididymis facilitates the storage of sperm by enhancing oxygen availability. Gamete Research, 15; 237-254.
  10. 1 2 Saint-Hilaire, M. (1827). Sur les appariels sexuels et urinaires de l’Ornithorhynque. Memoires du Museum d’Histoire Naturelle; 15, 1-48.
  11. 1 2 3 Oudemans. J.T. (1892). Die accessorishen Geschlechtsdrusen der Saugetthiere – Monotremata. Natuurkundige Verhandelingen van de Hollandsche Maatschappij der. Wetenschap Haarlem Verz. 3, Deel 5, 2 de Stuk; 11-14.
  12. 1 2 3 4 5 6 7 Temple-Smith, P. (1973). Season breeding biology of the platypus, Ornithorhynchis anatinus (Shaw, 1799), with special reference to the male. Ph.D. Thesis, Australian National University.
  13. 1 2 3 4 5 6 7 8 Djakiew, D. (1978). Studies of the Male Reproductive Tract of the Echidna (Tachyglossus aculeatus) with particular emphasis on the Epididymis. Honors Thesis, University of Newcastle, Australia.
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