Efficiency of Spermatogenesis: a Comparative Approach
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Animal Reproduction Science 60±61Ž. 2000 471±480 www.elsevier.comrlocateranireprosci Efficiency of spermatogenesis: a comparative approach L. Johnson a,c,), D.D. Varner b, M.E. Roberts a, T.L. Smith a, G.E. Keillor a, W.L. Scrutchfield b a Department of Veterinary Anatomy and Public Health, College of Veterinary Medicine, Texas A&M UniÕersity, College Station, TX 77843-4458, USA b Department of Large Animal Medicine and Surgery, College of Veterinary Medicine, Texas A&M UniÕersity, College Station, TX 77843-4458, USA c Center for EnÕironmental and Rural Health, College of Veterinary Medicine, Texas A&M UniÕersity, College Station, TX 77843-4458, USA Abstract Efficiency of spermatogenesis is the estimated number of spermatozoa produced per day per gram of testicular parenchyma. Spermatogenesis is the process of cell division and cell differentia- tion by which spermatozoa are produced in testes. Efficiency of spermatogenesis is influenced by species differences in the numerical density of germ cell nuclei and in the life span of these cells. Activities of spermatogonia, spermatocytes, and spermatids partition spermatogenesis into three major divisionsŽ. spermatocytogenesis, meiosis, and spermiogenesis, respectively . Spermatocyto- genesis involves mitotic germ cell division to produce stem cells and primary spermatocytes. Meiosis involves duplication of chromosomes, exchange of genetic material, and two cell divisions that reduce the chromosome number and yield four spermatids. In spermiogenesis, spherical spermatids differentiate into mature spermatids which are released in the lumen of seminiferous tubules as spermatozoa. Spermatogenesis and germ cell degeneration can be quanti- fied from numbers of germ cells in various developmental steps throughout spermatogenesis. Germ cell degeneration occurs throughout spermatogenesis; however, the greatest impact occurs during spermatocytogenesis and meiosis. There are species and seasonal influences on the developmental steps in spermatogenesis at which germ cell degeneration occurs. Number of Sertoli cells, amount of smooth endoplasmic reticulum of Leydig cells, and the number of missing generations of germ cells within the spermatogenic stage of the cycle influence efficiency of spermatogenesis. Efficiency of spermatogenesis is influenced to the amount of germ cell degenera- ) Corresponding author. Tel.: q1-979-845-9279; fax: q1-979-847-8981. E-mail address: [email protected]Ž. L. Johnson . 0378-4320r00r$ - see front matter q 2000 Published by Elsevier Science B.V. All rights reserved. PII: S0378-4320Ž. 00 00108-1 472 L. Johnson et al.rAnimal Reproduction Science 60±61() 2000 471±480 tion, pubertal development, season of the year, and aging of humans and animals. q 2000 Published by Elsevier Science B.V. All rights reserved. Keywords: Spermatogenesis; Species comparisons; Germ cell degeneration 1. Introduction 1.1. Definition and background Spermatogenesis is the sum total of the events that occur within the testis that produce spermatozoaŽ. Johnson, 1991b . Spermatogenesis occurs within seminiferous tubules of the testis. It is a lengthy, chronological process by which stem cell spermatogonia divide by mitosis to maintain their own numbers and to cyclically produce primary spermatocytes that undergo meiosis to produce haploid spermatids which differentiateŽ. without further division into spermatozoa. The efficiency of spermatogenesis is the number of spermatozoa produced per gram of testicular parenchyma and is not influenced by difference in testicular size among animals. Spermatocytogenesis, meiosis, and spermiogenesis are characterized by division andror differentiation of spermatogonia, spermatocytes, and spermatids, respectively, and are three major divisions of spermatogenesisŽ. Fig. 1 . In the bull, these divisions take 21, 23, and 17 days, respectively, for a total duration of 61 daysŽ Fig. 1; Amann, 1970. During spermatocytogenesis, stem cell spermatogonia divide by mitosis to produce other stem cells that continue the lineage throughout the adult life of malesŽ Fig. 1. Stem cells give rise to spermatogonia that cyclically produce committed spermatogo- nia which proliferate andror differentiate to produce primary spermatocytes that un- dergo meiosis. Meiosis allows exchange of genetic material between homologous chromosomes of primary spermatocytes and the production of haploid spermatidsŽ Fig. 1.Ž. During spermiogenesis Fig. 1 , spermatids differentiate from cells with spherical nuclei into mature germ cells shaped like spermatozoa for that species. The flagellum is developed into a tail, and the head of the spermatozoon is composed of the compressed nucleusŽ. source of the male genome and an acrosome with its enzymes necessary to penetrate the layers of the egg. 1.2. Kinetics of spermatogenesis The spermatogenic cycleŽ. cycle of the seminiferous epithelium is superimposed on the major divisions of spermatogenesisŽ spermatocytogenesis, meiosis, and spermiogene- sis; Fig. 1. The cycle of the seminiferous epithelium is ``a series of changes in a given areaŽ. region of seminiferous epithelium between two appearances of the same develop- mental stagesŽ.Ž steps '' Leblond and Clermont, 1952 . and lasts for 13.5 days in the bull. If spermiationŽ release of spermatozoa from seminiferous epithelium and counterpart to ovulation in the female. is used as a reference point, the spermatogenic cycle would be all the events that occur between two consecutive spermiations from a given region of the tubule. L. Johnson et al.rAnimal Reproduction Science 60±61() 2000 471±480 473 Fig. 1. Drawings and classification of germ cells at different developmental steps in the three major divisions of spermatogenesisŽ. spermatocytogenesis, meiosis, and spermiogenesis combined to make the eight stages of the cycle of bull seminiferous epithelium. During the 21 days of spermatocytogenesis, A spermatogoniaŽ. A enters cyclicŽ. at 13.5-day interval activity during stage III and undergo division to produce intermediate Ž. In , BŽ. B spermatogonia, and leptotene primary spermatocytes Ž. L . During the 23 days of meiosis, leptotene primary spermatocytes differentiate through zygoteneŽ. Z , pachytene Ž. P , and diplotene Ž. D before the first meiotic division to produce secondary spermatocytesŽ. SS , and the second meiotic division to produce Sa spermatidsŽ. Sa . During the 17 days of spermiogenesis, Sa spermatids differentiate through Sb11Ž. Sb , Sb 2 Ž.Sb21122 , Sc Ž. Sc , Sd Ž. Sd , and Sd Ž. Sd steps of development before spermiation as spermatozoa. The letters indicate the developmental step, and the numbers associated with each germ cell step indicate the developmen- tal age of each cell type in the middle of each spermatogenic stage. The cycle length is 13.5 days, and the duration of spermatogenesis is 61 days in the bull. Modified from Johnson et al.Ž. 1994 . The cycle length and frequency at which spermatozoa are released both are deter- mined by the rate at which committed spermatogonia enter the process of spermatogene- sis. The cycle length and duration of spermatogenesisŽ from the production of committed spermatogonia to spermiation.Ž are species-specific Swierstra et al, 1974; Amann, 1986 . The cycle length in days for the prairie vole is 7.2, hamster 8.7, mouse 8.9, rhesus monkey 9.5, rabbit 10.7, stallion 12.2, bull 13.5, beagle dog 13.6, and man 16 Ž.Clermont, 1963; Swierstra et al, 1974; Amann, 1981, 1986 . The stage represents an association of 4±5 germ cells, each of which is in a specific, chronological, developmental step in spermatogenesis. The assignment of stages repre- sent man-made divisions of naturally cyclically occurring cellular associations. In bulls, 474 L. Johnson et al.rAnimal Reproduction Science 60±61() 2000 471±480 the cycle has been divided into eight stagesŽ.Ž Amann, 1970 or 12 stages Berndtson and Desjardins, 1974.Ž. Fourteen stages have been described in rats Clermont, 1972 , eight in the horseŽ. Swierstra et al, 1974 , and only six stages in humans Ž. Clermont, 1963 . The bullŽ.Ž Amann, 1970 and horse Swierstra et al, 1974 . , like most species, have mainly only one stage of the cycle represented in a cross-section of the seminiferous tubule. Humans have more than two stages per cross-sectionŽ. Clermont, 1963 . 1.3. Testis Quantitative approaches have been extended to calculate daily sperm production, a quantitative measure of spermatogenesis to express the total number of spermatozoa produced per day by a testis or paired testesŽ Kennelly and Foote, 1964; Amann, 1970; Johnson, 1986b. Considering the life span and theoretical yield of a specific germ cell, a daily expression of spermatozoan production can be obtained from the number of germ cells of that type in the testisŽ. Kennelly and Foote, 1964; Amann, 1970 . The life span of a germ cell is the duration of stages of the cycle in which that cell type occurs. Theoretical yields are calculated by 2 n, where n is the number of cell divisions between that cell type and spermatids. Daily sperm production per gram of testicular parenchyma is a measure of efficiency of spermatogenesis, and it is useful in species comparisonsŽ Fig. 2; Amann et al, 1976; Fig. 2. Efficiency of spermatogenesis in various species based on potential daily sperm production per gram parenchyma at different developmental steps in spermatogenesis of the rat, bull, horse, boar, and human. Potential daily sperm production per gram is calculated from numbers of B spermatogonia, pachytene primary spermatocytes, Golgi and cap phase spermatidsŽ.