ANNALS OF HUMAN BIOLOGY, 1977, VOL. 4, NO. 4, 3 8 9 - 3 9 2
LETTERS
TO THE
EDITOR
Time of fertilization and sex ratio of offspring
Ann Hum Biol Downloaded from informahealthcare.com by York University Libraries on 12/30/14 For personal use only.
30 March 1977 Dear Sir, In his recent paper 'Time of Fertilization and Sex Ratio of Offspring--a Review, the author, William H. James (1976) refers to an earlier paper by myself 'Relation of Time of Conception during the Estrous Cycle to the Sex Ratio'. In this paper I give a direct quote, word for word, of a paragraph from a paper by the famous biostatistician and geneticist Raymond Pearl (1917) as follows : "Some earlier statistics seemed to indicate that there is a possibility of influencing the sex ratio at different parts of the heat period. However, with more extensive statistics at hand, it appears conclusively established that there is no definite permanent relation between the time in the heat period at which the cow is serviced and the sex of the offspring. The apparent relationship between these two, factors which is believed by many breeders to exist and which our earlier statistics appeared to indicate, seems now to be purely accidental, and to have arisen only because of the comparative meagerness of the statistics on which the matter was discussed". As this is a direct quote from Pearl (1917), it is a mystery to me as to why Dr. James concluded "Bernstein (1952) had erroneously denied that the data of Pearl (1917) offered any support to the hypothesis". Nevertheless, it was a pleasure to find that James (1976) agrees with my theorem (1958) that the high secondary sex ratios observed at the end of World War 2 and for 18 months after the armistice can best be attributed to an increase (in percentage terms) in the births from fathers who are quickly fertile and thus have a sex ratio among offspring above the average. I myself used the more lady-like expression 'sexual drive' rather than 'coital rate' but otherwise our sentences are almost identical. Most sincerely, Marianne E. Bernstein-Wiener, MCZ Laboratories, Harvard University.
References Bernstein, M. E. (1952). Relation of time of conception during estrus cycle to the sex ratio. Journal of Heredity. 43, 69-71. Bernstein, M. E. (1958). A genetic explanation of the wartime increase in the secondary sex ratio. American Journal of Human Genetics, 10, 68-70. James, W. H. (1976). Timing of fertilization and sex ratio of offspring. Annals of Human Biology, 3, 549-556. Pearl, R. (1917). Maine Agricultural Station Annual Report, Bull. No. 261. part 3.
Dr. James has replied as follows: Dear Sir, Pearl's (1917) data were as follows:
Sex ratio of offspring
N
Cows served early in heat
0.51
392
Cows served in the middle of heat
0. 517
522
Cows served late in heat
0. 469
399
Ann Hum Biol Downloaded from informahealthcare.com by York University Libraries on 12/30/14 For personal use only.
390
Letters to the Editor
The hypothesis at issue is that with natural insemination, males are conceived earlier in the cycle than females on the average. Pearl may have denied it, but these data do give some (admittedly weak) support to the hypothesis. It may be useful if I try to summarize the difference between Dr. Bernstein's hypothesis and mine. She and I agree that children of highly fecund couples have slightly higher sex ratios than the children of other couples. Our explanations of this phenomenon are, however, different. Dr. Bernstein, as I understand her, suggests that this difference exists for undefined genetic reasons. I have suggested that part of the reason is that (a) Time of insemination is related to sex of the resulting zygote, early inseminations producing a higher proportion of males, and (b) Therefore coital rates are related to the sex of the zygote, higher rates producing more males. (c) Highly fecund couples have higher coital rates than other couples and for that reason they produce a slightly higher proportion of boys. The following is a list of the principal findings which seem to be subsumed or explained by my hypothesis but not by Dr. Bernstein's (references substantiating these findings are in my review (James, 1976 a))" (1) The direct data suggesting that there is a relationship between time of insemination and sex of the resulting zygote. (2) The suggestion that the decline in sex ratio with maternal age is partially secondary to that with paternal age. (3) The evidence of departures from binomial expectation in the distributions of the combinations of the sexes in litters of some mammalian species (James, 1975 a, 1976 b), and in h u m a n dizygotic twins (James, 1976 c). I should add that it is no part of my case that Dr. Berstein's hypothesis is false. I have estimated (James, 1975 b) that the Lexis variation in Pma~ between h u m a n couples seems considerably to exceed that which may be attributed to variation in coital rate. W h a t I a m contending is that, irrespective of Dr. Bernstein's hypothesis, mine is true. William H. James, University College London.
References James, W. H. (1975 a). Distributions of the combinations of the sexes in mammalian litters. Genetical Research, 26, 45-53. James, W. H. (1975 b). Sex ratio and the sex composition of the existing sibs. Annals of Human Genetics, 38, 371-378. James, W. H. (1976 a). Timing of fertilization and sex ratio of offspring--a review. Annals of Human Biology, 3, 549-556. James, W. H. (1976 b). The combinations of the sexes in twin lambings. Genetical Research, 28, 277-280. James, W. H. (1976 c). The possibility of a flaw underlying Weinberg's Differential Rule. Annals of Human Genetics, 40, 197-199.
The primary sex ratio of man
Dear Sir, Matthiessen and Matthiessen (Vol. 4, pages 183-185) discussed the hypothesis that there is a large excess o f male conceptions which are preferentially lost by spontaneous abortion, leaving a slightly raised sex ratio of about 106 males to 100 females at term. This idea originally sprang from studies of spontaneous and induced abortions based upon sex-chromatin determination. More recent studies, employing full karyotype analysis, have shown that about 20 per cent of spontaneous abortions have a 45,X karyotype and are sex-chromatin negative, although phenotypically female. Other chromosomal abnormalities, such as 69,XXY triploidy, also affect the sex-chromatin results. These studies have recently been summarized by Boue (1976) in the present context. The data shown in table 1 give a sex ratio of 109.25 for more than two thousand chromosomally normal spontaneous abortions.
Letters to the Editor Location U.K. U.K. U.S.A. Canada Switzerland France Denmark
Ann Hum Biol Downloaded from informahealthcare.com by York University Libraries on 12/30/14 For personal use only.
Total
391
46,XY
46,XX
Sex ratio
365 226 42 38 92 281 54
289 193 37 34 95 296 61
126.3 117.1 113.5 111.8 96.8 94.9 88.5
1098
1005
109.25
Table 1. Sex ratio of chromosomally normal spontaneous abortions from full karyotype studies (Bou6, 1976; Dhadial, Machin and Tait, 1970; Alberman, personal communication). The highest sex ratios were obtained by studies from this laboratory (Dhadial, Machin and Tait, 1970; Creasy, Crolla and Alberman, 1976) which included abortuses expelled at the end of the second trimester. In the larger of these studies the sex-ratio was 126.3, but when abortions after the nineteenth week were excluded this fell to 114.8. The late abortions resembled stillbirths more than earlier abortions in the type and prevalence of chromosome abnormalities and physical malformations, and the risk of stillbirth is known to be greater for male than for female fetuses (Chamberlain, Chamberlain, Howlett and Claireux, 1976). Conversely, the studies which concentrated on earlier abortions (those undertaken in France, Denmark and Switzerland) produced the lowest sex-ratios. Professor Bou6 also summarized the available information for induced abortions, and found a sex-ratio of 96.2 based on full chromosome analysis of 3496 terminations. Most histological studies of the gonads of abortuses have indicated a high sex ratio, with the notable exception of the very
Table 2.
Location
XY
XX
Sex ratio
Denmark Canada U.K. France U.K.
32 21 58 217 24
27 19 64 275 35
118.5 110.5 90.6 78.9 68.6
Total
352
420
83.8
Sex ratio of trisomic spontaneous abortions. (Same sources as Table 1).
large study by Tietze (1948) which derived a ratio of 107.9 from nearly six thousand abortions which were "mostly unintentional". A high sex-ratio was also obtained by many of the early sex chromatin studies of induced abortions, but, as the Matthiessens stated, a more recent study by Bochkov and Kostrova (1973) produced a ratio of 103.4 from 3000 specimens. Thus although there is a wide variation in the reported sex ratios of spontaneous and induced abortions, there seems to be no good reason for believing in a large excess of male spontaneous abortions, and hence a distorted primary sex ratio. The sex-specific mortality rates may well be different in early pregnancy, but the excess of male deaths during late pregnancy and early infancy may merely counterbalance a previous small excess of female deaths. In this context it is interesting that there may be a low sex-ratio amongst trisomic conceptuses, which are mostly lost during the early stages of gestation (table 2). M. R. Creasy, Paediatric Research Unit, The Prince Philip Research Laboratories, Guy's Hospital Medical School, l l May 1977 London SEI 9RT.
References Bochkov, N. P. and Kostrova, A. A. (1973). Sex-ratio among human embryos and newborn in a Russian population. Human Genetics, 17, 91-98. Bou6, A. (1976). L'exc~s de conceptus males. La surmortalit6 des embryous males : realit6 ou mythe ? La Nouvelle Presse Mddicale, 5, 1307.
392
Letters to the Editor
Ann Hum Biol Downloaded from informahealthcare.com by York University Libraries on 12/30/14 For personal use only.
Chamberlain, R., Chamberlain, G., Howlett, B., and Claireaux, A. (1976). British Births 1970 Volume 1. The First Week of Life. London, Heinemann. Creasy, M. R., Crolla, J. A., and Alberman, E. D. (1976). A cytogenetic study of human spontaneous abortions using banding techniques. Human Gentics, 31, 177-196. Dhadial, R. K., Machin, A. M., and Tait, S. M. (1970). Chromosomal anomalies in spontaneously aborted human fetuses. Lancet, ii, 20-21. Tietze, C. (1948). A note on the sex ratio of abortions. Human Biology, 20, 156-160.
Forthcoming papers The following papers will appear in forthcoming issues of Annals of Human Biology:
Ljung, B.-O., Fischbein, S., and Lindgren, G. A comparison of twins and singleton controls of matched age followed longitudinally from 10 to 18 years. Fischbein, S. Intra-pair similarity in physical growth of monozygotic and of dizygotic twins during puberty. Buckler, J. M. H., and Brodie, D.A. Barua, D., and Paguio, A. S.
Growth and maturity characteristics of schoolboy gymnasts.
ABO blood groups and cholera.
Malina, R. M., Chumlea, C., and Lopez, F. G. Age at menarche in Oaxaca, Mexico, schoolgirls, with comparative data for other areas of Mexico. Malina, R. M., and Chumlea, C. Age at menarche in deaf girls. Ramesh, A., and Murty, J.S.
Variation and inheritance of relative length of index finger in man.
Raja, C., Singh, R., and Bharadwaj, H. Anthropometric determination of body volume, body density and segmental volume in adult Indian women. Kimura, K. Skeletal maturity of the hand and wrist in Japanese children in Sapporo by the TW2 method. Mitchell, R. J., and Cook, R.M. Phenylthiocarbamide (PTC) taste sensitivity in selected populations of the Isle of Man and Cumbria. Mitchell, R.J.
Red-green colour blindness in the Isle of Man and Cumbria.
Brackenridge, C.J.
The secular variation of Australian twin births over fifty years.
Togo, M., Morinaga, E., and Togo, T. A cohort observation of urinary hydroxyproline, creatinine and urea excretion during the growth of five siblings. Brown, W. J., and Jones, P. R.M.
The distribution of body fat in relation to habitual activity.
Van't Hof, M. A., and Roede, M . J . A Monte Carlo test of weight as a critical factor in menarche compared with bone age, and measures of height, weight and sexual development.
LETTERS
TO THE
EDITOR
Time of fertilization and sex ratio of offspring
Ann Hum Biol Downloaded from informahealthcare.com by York University Libraries on 12/30/14 For personal use only.
30 March 1977 Dear Sir, In his recent paper 'Time of Fertilization and Sex Ratio of Offspring--a Review, the author, William H. James (1976) refers to an earlier paper by myself 'Relation of Time of Conception during the Estrous Cycle to the Sex Ratio'. In this paper I give a direct quote, word for word, of a paragraph from a paper by the famous biostatistician and geneticist Raymond Pearl (1917) as follows : "Some earlier statistics seemed to indicate that there is a possibility of influencing the sex ratio at different parts of the heat period. However, with more extensive statistics at hand, it appears conclusively established that there is no definite permanent relation between the time in the heat period at which the cow is serviced and the sex of the offspring. The apparent relationship between these two, factors which is believed by many breeders to exist and which our earlier statistics appeared to indicate, seems now to be purely accidental, and to have arisen only because of the comparative meagerness of the statistics on which the matter was discussed". As this is a direct quote from Pearl (1917), it is a mystery to me as to why Dr. James concluded "Bernstein (1952) had erroneously denied that the data of Pearl (1917) offered any support to the hypothesis". Nevertheless, it was a pleasure to find that James (1976) agrees with my theorem (1958) that the high secondary sex ratios observed at the end of World War 2 and for 18 months after the armistice can best be attributed to an increase (in percentage terms) in the births from fathers who are quickly fertile and thus have a sex ratio among offspring above the average. I myself used the more lady-like expression 'sexual drive' rather than 'coital rate' but otherwise our sentences are almost identical. Most sincerely, Marianne E. Bernstein-Wiener, MCZ Laboratories, Harvard University.
References Bernstein, M. E. (1952). Relation of time of conception during estrus cycle to the sex ratio. Journal of Heredity. 43, 69-71. Bernstein, M. E. (1958). A genetic explanation of the wartime increase in the secondary sex ratio. American Journal of Human Genetics, 10, 68-70. James, W. H. (1976). Timing of fertilization and sex ratio of offspring. Annals of Human Biology, 3, 549-556. Pearl, R. (1917). Maine Agricultural Station Annual Report, Bull. No. 261. part 3.
Dr. James has replied as follows: Dear Sir, Pearl's (1917) data were as follows:
Sex ratio of offspring
N
Cows served early in heat
0.51
392
Cows served in the middle of heat
0. 517
522
Cows served late in heat
0. 469
399
Ann Hum Biol Downloaded from informahealthcare.com by York University Libraries on 12/30/14 For personal use only.
390
Letters to the Editor
The hypothesis at issue is that with natural insemination, males are conceived earlier in the cycle than females on the average. Pearl may have denied it, but these data do give some (admittedly weak) support to the hypothesis. It may be useful if I try to summarize the difference between Dr. Bernstein's hypothesis and mine. She and I agree that children of highly fecund couples have slightly higher sex ratios than the children of other couples. Our explanations of this phenomenon are, however, different. Dr. Bernstein, as I understand her, suggests that this difference exists for undefined genetic reasons. I have suggested that part of the reason is that (a) Time of insemination is related to sex of the resulting zygote, early inseminations producing a higher proportion of males, and (b) Therefore coital rates are related to the sex of the zygote, higher rates producing more males. (c) Highly fecund couples have higher coital rates than other couples and for that reason they produce a slightly higher proportion of boys. The following is a list of the principal findings which seem to be subsumed or explained by my hypothesis but not by Dr. Bernstein's (references substantiating these findings are in my review (James, 1976 a))" (1) The direct data suggesting that there is a relationship between time of insemination and sex of the resulting zygote. (2) The suggestion that the decline in sex ratio with maternal age is partially secondary to that with paternal age. (3) The evidence of departures from binomial expectation in the distributions of the combinations of the sexes in litters of some mammalian species (James, 1975 a, 1976 b), and in h u m a n dizygotic twins (James, 1976 c). I should add that it is no part of my case that Dr. Berstein's hypothesis is false. I have estimated (James, 1975 b) that the Lexis variation in Pma~ between h u m a n couples seems considerably to exceed that which may be attributed to variation in coital rate. W h a t I a m contending is that, irrespective of Dr. Bernstein's hypothesis, mine is true. William H. James, University College London.
References James, W. H. (1975 a). Distributions of the combinations of the sexes in mammalian litters. Genetical Research, 26, 45-53. James, W. H. (1975 b). Sex ratio and the sex composition of the existing sibs. Annals of Human Genetics, 38, 371-378. James, W. H. (1976 a). Timing of fertilization and sex ratio of offspring--a review. Annals of Human Biology, 3, 549-556. James, W. H. (1976 b). The combinations of the sexes in twin lambings. Genetical Research, 28, 277-280. James, W. H. (1976 c). The possibility of a flaw underlying Weinberg's Differential Rule. Annals of Human Genetics, 40, 197-199.
The primary sex ratio of man
Dear Sir, Matthiessen and Matthiessen (Vol. 4, pages 183-185) discussed the hypothesis that there is a large excess o f male conceptions which are preferentially lost by spontaneous abortion, leaving a slightly raised sex ratio of about 106 males to 100 females at term. This idea originally sprang from studies of spontaneous and induced abortions based upon sex-chromatin determination. More recent studies, employing full karyotype analysis, have shown that about 20 per cent of spontaneous abortions have a 45,X karyotype and are sex-chromatin negative, although phenotypically female. Other chromosomal abnormalities, such as 69,XXY triploidy, also affect the sex-chromatin results. These studies have recently been summarized by Boue (1976) in the present context. The data shown in table 1 give a sex ratio of 109.25 for more than two thousand chromosomally normal spontaneous abortions.
Letters to the Editor Location U.K. U.K. U.S.A. Canada Switzerland France Denmark
Ann Hum Biol Downloaded from informahealthcare.com by York University Libraries on 12/30/14 For personal use only.
Total
391
46,XY
46,XX
Sex ratio
365 226 42 38 92 281 54
289 193 37 34 95 296 61
126.3 117.1 113.5 111.8 96.8 94.9 88.5
1098
1005
109.25
Table 1. Sex ratio of chromosomally normal spontaneous abortions from full karyotype studies (Bou6, 1976; Dhadial, Machin and Tait, 1970; Alberman, personal communication). The highest sex ratios were obtained by studies from this laboratory (Dhadial, Machin and Tait, 1970; Creasy, Crolla and Alberman, 1976) which included abortuses expelled at the end of the second trimester. In the larger of these studies the sex-ratio was 126.3, but when abortions after the nineteenth week were excluded this fell to 114.8. The late abortions resembled stillbirths more than earlier abortions in the type and prevalence of chromosome abnormalities and physical malformations, and the risk of stillbirth is known to be greater for male than for female fetuses (Chamberlain, Chamberlain, Howlett and Claireux, 1976). Conversely, the studies which concentrated on earlier abortions (those undertaken in France, Denmark and Switzerland) produced the lowest sex-ratios. Professor Bou6 also summarized the available information for induced abortions, and found a sex-ratio of 96.2 based on full chromosome analysis of 3496 terminations. Most histological studies of the gonads of abortuses have indicated a high sex ratio, with the notable exception of the very
Table 2.
Location
XY
XX
Sex ratio
Denmark Canada U.K. France U.K.
32 21 58 217 24
27 19 64 275 35
118.5 110.5 90.6 78.9 68.6
Total
352
420
83.8
Sex ratio of trisomic spontaneous abortions. (Same sources as Table 1).
large study by Tietze (1948) which derived a ratio of 107.9 from nearly six thousand abortions which were "mostly unintentional". A high sex-ratio was also obtained by many of the early sex chromatin studies of induced abortions, but, as the Matthiessens stated, a more recent study by Bochkov and Kostrova (1973) produced a ratio of 103.4 from 3000 specimens. Thus although there is a wide variation in the reported sex ratios of spontaneous and induced abortions, there seems to be no good reason for believing in a large excess of male spontaneous abortions, and hence a distorted primary sex ratio. The sex-specific mortality rates may well be different in early pregnancy, but the excess of male deaths during late pregnancy and early infancy may merely counterbalance a previous small excess of female deaths. In this context it is interesting that there may be a low sex-ratio amongst trisomic conceptuses, which are mostly lost during the early stages of gestation (table 2). M. R. Creasy, Paediatric Research Unit, The Prince Philip Research Laboratories, Guy's Hospital Medical School, l l May 1977 London SEI 9RT.
References Bochkov, N. P. and Kostrova, A. A. (1973). Sex-ratio among human embryos and newborn in a Russian population. Human Genetics, 17, 91-98. Bou6, A. (1976). L'exc~s de conceptus males. La surmortalit6 des embryous males : realit6 ou mythe ? La Nouvelle Presse Mddicale, 5, 1307.
392
Letters to the Editor
Ann Hum Biol Downloaded from informahealthcare.com by York University Libraries on 12/30/14 For personal use only.
Chamberlain, R., Chamberlain, G., Howlett, B., and Claireaux, A. (1976). British Births 1970 Volume 1. The First Week of Life. London, Heinemann. Creasy, M. R., Crolla, J. A., and Alberman, E. D. (1976). A cytogenetic study of human spontaneous abortions using banding techniques. Human Gentics, 31, 177-196. Dhadial, R. K., Machin, A. M., and Tait, S. M. (1970). Chromosomal anomalies in spontaneously aborted human fetuses. Lancet, ii, 20-21. Tietze, C. (1948). A note on the sex ratio of abortions. Human Biology, 20, 156-160.
Forthcoming papers The following papers will appear in forthcoming issues of Annals of Human Biology:
Ljung, B.-O., Fischbein, S., and Lindgren, G. A comparison of twins and singleton controls of matched age followed longitudinally from 10 to 18 years. Fischbein, S. Intra-pair similarity in physical growth of monozygotic and of dizygotic twins during puberty. Buckler, J. M. H., and Brodie, D.A. Barua, D., and Paguio, A. S.
Growth and maturity characteristics of schoolboy gymnasts.
ABO blood groups and cholera.
Malina, R. M., Chumlea, C., and Lopez, F. G. Age at menarche in Oaxaca, Mexico, schoolgirls, with comparative data for other areas of Mexico. Malina, R. M., and Chumlea, C. Age at menarche in deaf girls. Ramesh, A., and Murty, J.S.
Variation and inheritance of relative length of index finger in man.
Raja, C., Singh, R., and Bharadwaj, H. Anthropometric determination of body volume, body density and segmental volume in adult Indian women. Kimura, K. Skeletal maturity of the hand and wrist in Japanese children in Sapporo by the TW2 method. Mitchell, R. J., and Cook, R.M. Phenylthiocarbamide (PTC) taste sensitivity in selected populations of the Isle of Man and Cumbria. Mitchell, R.J.
Red-green colour blindness in the Isle of Man and Cumbria.
Brackenridge, C.J.
The secular variation of Australian twin births over fifty years.
Togo, M., Morinaga, E., and Togo, T. A cohort observation of urinary hydroxyproline, creatinine and urea excretion during the growth of five siblings. Brown, W. J., and Jones, P. R.M.
The distribution of body fat in relation to habitual activity.
Van't Hof, M. A., and Roede, M . J . A Monte Carlo test of weight as a critical factor in menarche compared with bone age, and measures of height, weight and sexual development.
