Genetic control of recombination in the silkworm

Genetic control of recombination in the silkworm

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ABSTRACT Summary Response to selection for particular rates of recombination in the silkworm (_Bombyx mori_) is rapid; from a highly heterogeneous foundation stock Hasimoto achieved, in only 10 generations, a 32 per cent difference between lines selected for high and low recombination between the dominant markers _Striped_ and _Yellow_ in chromosome 2. The present study analyses the difference between Hasimoto’s high and low stocks by means of a set of four factorial F1 crosses, and all but one of the corresponding eight backcrosses. As there is no recombination in females this method can distinguish the effects on recombination of (i) a large inversion in the marked chromosome (chromosome 2), (ii) genes or small inversions in chromosome 2, (iii) genes in the sex chromosome, (iv) genes in the other autosomes, (v) the cytoplasm. There is no large inversion causing reduced recombination in chromosome 2; the cytoplasm has little, if any effect. A recombination gene (or genes, the analysis does not distinguish) is located in chromosome 2, the _high_ allele being recessive (effect of 6 to 11 per cent). At least one other autosome carries a similar gene, with _high_ recessive (effect of around 8 per cent), and there also appears to be an autosome (or several autosomes) with a _low_ recessive effect of 9 per cent, which may or may not be identical with the other autosome. Further autosomes might be revealed by a more sensitive analysis. There may be a small effect (_high_ recessive) due to the X chromosome. There is no overall dominance in the genes controlling recombination. The genes appear to be either of the _rec_ type discovered in _Neurospora_, or general modifiers of genomic recombination. Although supergenes in mimetic butterflies at least do not arise by the tightening of linkage between loosely linked or independent loci, modifiers of the type demonstrated in _Bombyx_ may be very effective in tightening still further the linkage within supergenes that come into existence by the alternative “sieve“ mechanism. If most modifiers of recombination are general in their action, rather than specific to one short length of chromosome, then this may in part explain why the genome does not congeal. SIMILAR CONTENT BEING VIEWED BY OTHERS LONG-TERM EXHAUSTION OF THE INBREEDING LOAD IN _DROSOPHILA MELANOGASTER_ Article Open access 16 August 2021 DETECTING PURGING OF INBREEDING DEPRESSION BY A SLOW RATE OF INBREEDING FOR VARIOUS TRAITS: THE IMPACT OF ENVIRONMENTAL AND EXPERIMENTAL CONDITIONS Article 26 April 2021 ANEUPLOIDY AND PLOIDY VARIATION CONDITIONED BY THE B CHROMOSOME OF MAIZE Article Open access 25 April 2025 ARTICLE PDF REFERENCES * Abdullah, N F, and Charlesworth, B. 1974. Selection for reduced crossing over in _Drosophila melanogaster_. _Genetics_, 76, 447–451. CAS  PubMed  PubMed Central  Google Scholar  * Acton, A B. 1961. An unsuccessful attempt to reduce recombination by selection. _Amer Natur_, 95, 119–120. Article  Google Scholar  * Allard, R W. 1963. Evidence for genetic restriction of recombination in the lima bean. _Genetics_, 48, 1389–1395. CAS  PubMed  PubMed Central  Google Scholar  * Ayuzawa, CH, Sekodo, I, Yamakawa, K, Sakukai, U, Kurata, W, Yaginuma, Y, and Tokoro, Y. 1972. _Handbook of Silkworm Rearing Agricultural Technique Manual_. Fuji Publishing Co. Ltd., Tokyo. Google Scholar  * De Boer, R, and Van Der Hoeven, F A. 1977. Son-sire regression based on heritability estimates of chiasma frequency, using T7OH mouse translocation hctcrozygotes, and the relation between univalence, chiasma frequency and sperm production. _Heredity_, 39, 335–343. Article  CAS  PubMed  Google Scholar  * Catcheside, D G. 1977. _The Genetics of Recombination_. Arnold, London. Google Scholar  * Charlesworth, B, and Charlesworth, D. 1976. Theoretical genetics of Batesian mimicry. II. Evolution of supergenes. _J Theor Biol_, 55, 305–324. Article  Google Scholar  * Chikushi, H. 1972. _Genes and Genetical Stocks of the Silkworm (Studies of Stock Culture in Biological Field No 1)_. Keigaku, Tokyo. Google Scholar  * Chinnici, J P. 1971a. Modification of recombination frequency in Drosophila. I. Selection for increased and decreased crossing over. _Genetics_, 69, 71–83. CAS  PubMed  PubMed Central  Google Scholar  * Chinnici, J P. 1971b. Modification of recombination frequency in Drosophila. II. The polygenic control of crossing over. _Genetics_, 69, 85–96. CAS  PubMed  PubMed Central  Google Scholar  * Clarke, C A, and Sheppard, P M. 1971. Further studies on the genetics of the mimetic butterfly _Papilio memnon_ L. _Phil Trans Roy Soc London B_, 263, 35–70. Article  Google Scholar  * Clarke, C A, and Sheppard, P M. 1972. The genetics of the mimetic butterfly _Popilio polytcs_ L. _Phil Trans Roy Soc London B_, 263, 431–458. Article  CAS  PubMed  Google Scholar  * Clarke, C A, and Sheppard, P M. 1977. A new tailed female form of _Papilio memnon_ L. and its probable genetic control. _Syst Entomol_, 2, 17–19. Article  Google Scholar  * Clarke, C A, Sheppard, P M, and Thornton, I W B. 1968. The genetics of the mimetic butterfly _Papilio memnon_ L. _Phil Trans Roy Soc London B_, 254, 37–89. Article  Google Scholar  * Dewees, A A. 1975. Genetic modification of recombination rate in _Tribolium castaneum_. _Genetics_, 81, 537–552. CAS  PubMed  PubMed Central  Google Scholar  * Dryja, A. 1959. Badania nad polimorfizmem Kraśnika Zmiennego (_Zygaena ephialtes_ L.). (Genetical investigation on the polymorphism of _Zygaena ephialtes_ L.). _Panstwowe Wydawnictwo Naukowe_, Warszawa, pp. 401 + folder of 12 plates and tables. * Emsley, M G. 1965. The geographical distribution of the color-pattern components of _Heliconius erato_ and _Heliconius melpomcne_ with gcnctical evidence for the systematic relationship between the two species. _Zoologica (New York)_, 49, 245–286. Google Scholar  * Fisher, R A. 1930. _The Gcnetical Theory of Natural Selection_. Clarendon Press, Oxford. Google Scholar  * Hasimoto, H. 1960. Selection of crossover value between _Striped_ and _Yellow_ in the silkworm. _11ème Conference Technique Sericicole Internationale, Murcie (Espagne)_, 365–367. * Kidwell, M G. 1972a. Genetic change of recombination value in _Drosophila melanogaster_. I. Artificial selection for high and low recombination and some properties of recombination-modifying genes. _Genetics_, 70, 419–432. CAS  PubMed  PubMed Central  Google Scholar  * Kidwell, M G. 1972b. Genetic change of recombination value in _Drosophila melanogaster_. II. Simulated natural selection. _Genetics_, 70, 433–443. CAS  PubMed  PubMed Central  Google Scholar  * Maynard Smith, J. 1977. Why the genome does not congeal. _Nature_, 268, 693–696. Article  Google Scholar  * Maynard Smith, J. 1978. _The Evolution of Sex_. Cambridge University Press, London. Google Scholar  * Nei, M. 1969. Linkage modification and sex difference in recombination. _Genetics_, 63, 681–699. CAS  PubMed  PubMed Central  Google Scholar  * Parsons, P A. 1958. Selection for increased recombination in _Drosophila melanogaster_. _Amer Natur_, 92, 255–256. Article  Google Scholar  * Schapp, T. 1978. Why should the genome congeal? _Nature_, 276, 535–536. Article  Google Scholar  * Shaw, D D. 1972. Genetic and environmental components of chiasma control. II. The response to selection in _Schistocerca_. _Chromosoma_, 37, 297–308. Article  CAS  PubMed  Google Scholar  * Sheppard, P M. 1975. _Natural Selection and Heredity_, fourth edition. Hutchinson, London. Google Scholar  * Sturtevant, A H. 1915. No crossing over in the female of the silkworm moth. _Amer Natur_, 49, 42–44. Article  Google Scholar  * Suomalainen, E. 1965. On the chromosomes of the Geometrid moth genus _Cidaria_. _Chromosorna (Berlin)_, 16, 166–184. Article  Google Scholar  * Suomalainen, E, Cook, L H, and Turner, J R G. 1973. Achiasmatic oogenesis in the heliconiine butterflies. _Hereditas_, 74, 302–304. Article  Google Scholar  * Traut, W. 1977. A study of recombination, formation of chiasmata and synaptonemal complexes in female and male meiosis of _Ephestia kuehniella_ (Lepidoptera). _Genetica_, 47, 135–142. Article  Google Scholar  * Turner, J R G. 1971. Studies of Müllerian mimicry and its evolution in burnet moths and heliconid butterflies. In _Ecological Genetics and Evolution_, ed. E. R. Creed, pp. 224–260. Blackwell Scientific Publications, Oxford. Chapter  Google Scholar  * Turner, J R G. 1975. A tale of two butterflies. _Natural History_, 84 (2), 28–37. Google Scholar  * Turner, J R G. 1976. Muellerian mimicry: classical “beanbag” evolution, and the role of ecological islands in adaptive race formation. In _Population Genetics and Ecology_, ed. S. Karlin and E. Nevo, pp. 185–218. Academic Press, New York and London. Google Scholar  * Turner, J R G. 1977. Butterfly mimicry: the genetical evolution of an adaptation. _Evol Biol_, 10, 163–206. Google Scholar  * Turner, J R G, and Crane, J. 1962. The genetics of some polymorphic forms of the butterflies _Heliconius melpomene_ Linnaeus and _H. erato_ Linnaeus. I. Major genes. _Zoologica (New York)_, 47, 141–152. Google Scholar  * Turner, J R G, Johnson, M S, and Eanes, W F. 1979. Contrasted modes of evolution in the same genome: allozymes and adaptive change in _Heliconius_. _Proc Natl Acad Sci USA_, 76, 1924–1928. Article  CAS  PubMed  PubMed Central  Google Scholar  * Turner, J R G, and Sheppard, P M. 1975. Absence of crossing-over in female butterflies (_Heliconius_). _Heredity_, 34, 265–269. Article  PubMed  Google Scholar  Download references ACKNOWLEDGEMENTS Acknowledgments.-The progress of this work has been dependent on the considerable skills of Mr Mart Koello, who adapted the Japanese techniques of silkworm rearing to our needs, and oversaw the rearing of the broods ; he is co-author of section 3. Much additional help was provided by Dr Charles Mitter, Mr Craig Sargent and Ms Melody Wolstoff. To all these people I am extremely grateful. I am much indebted to Professor Hiroshi Doira who provided several batches of the high and low stocks from Kyushu University. The research was supported by grant 5 ROI GM 20702 from the National Institutes of Health. AUTHOR INFORMATION Author notes * John R G Turner Present address: Department of Genetics, University of Leeds, Leeds, LS2 9JT, England AUTHORS AND AFFILIATIONS * Department of Ecology and Evolution, State University of New York, Stony Brook, 11794, N.Y., USA John R G Turner Authors * John R G Turner View author publications You can also search for this author inPubMed Google Scholar ADDITIONAL INFORMATION Contribution number 318 from the Program in Ecology and Evolution of the State University of New York at Stony Brook. RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Turner, J. Genetic control of recombination in the silkworm. _Heredity_ 43, 273–293 (1979). https://doi.org/10.1038/hdy.1979.83 Download citation * Received: 26 March 1979 * Issue Date: 01 October 1979 * DOI: https://doi.org/10.1038/hdy.1979.83 SHARE THIS ARTICLE Anyone you share the following link with will be able to read this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to clipboard Provided by the Springer Nature SharedIt content-sharing initiative

ABSTRACT Summary Response to selection for particular rates of recombination in the silkworm (_Bombyx mori_) is rapid; from a highly heterogeneous foundation stock Hasimoto achieved, in only


10 generations, a 32 per cent difference between lines selected for high and low recombination between the dominant markers _Striped_ and _Yellow_ in chromosome 2. The present study


analyses the difference between Hasimoto’s high and low stocks by means of a set of four factorial F1 crosses, and all but one of the corresponding eight backcrosses. As there is no


recombination in females this method can distinguish the effects on recombination of (i) a large inversion in the marked chromosome (chromosome 2), (ii) genes or small inversions in


chromosome 2, (iii) genes in the sex chromosome, (iv) genes in the other autosomes, (v) the cytoplasm. There is no large inversion causing reduced recombination in chromosome 2; the


cytoplasm has little, if any effect. A recombination gene (or genes, the analysis does not distinguish) is located in chromosome 2, the _high_ allele being recessive (effect of 6 to 11 per


cent). At least one other autosome carries a similar gene, with _high_ recessive (effect of around 8 per cent), and there also appears to be an autosome (or several autosomes) with a _low_


recessive effect of 9 per cent, which may or may not be identical with the other autosome. Further autosomes might be revealed by a more sensitive analysis. There may be a small effect


(_high_ recessive) due to the X chromosome. There is no overall dominance in the genes controlling recombination. The genes appear to be either of the _rec_ type discovered in _Neurospora_,


or general modifiers of genomic recombination. Although supergenes in mimetic butterflies at least do not arise by the tightening of linkage between loosely linked or independent loci,


modifiers of the type demonstrated in _Bombyx_ may be very effective in tightening still further the linkage within supergenes that come into existence by the alternative “sieve“ mechanism.


If most modifiers of recombination are general in their action, rather than specific to one short length of chromosome, then this may in part explain why the genome does not congeal. SIMILAR


CONTENT BEING VIEWED BY OTHERS LONG-TERM EXHAUSTION OF THE INBREEDING LOAD IN _DROSOPHILA MELANOGASTER_ Article Open access 16 August 2021 DETECTING PURGING OF INBREEDING DEPRESSION BY A


SLOW RATE OF INBREEDING FOR VARIOUS TRAITS: THE IMPACT OF ENVIRONMENTAL AND EXPERIMENTAL CONDITIONS Article 26 April 2021 ANEUPLOIDY AND PLOIDY VARIATION CONDITIONED BY THE B CHROMOSOME OF


MAIZE Article Open access 25 April 2025 ARTICLE PDF REFERENCES * Abdullah, N F, and Charlesworth, B. 1974. Selection for reduced crossing over in _Drosophila melanogaster_. _Genetics_, 76,


447–451. CAS  PubMed  PubMed Central  Google Scholar  * Acton, A B. 1961. An unsuccessful attempt to reduce recombination by selection. _Amer Natur_, 95, 119–120. Article  Google Scholar  *


Allard, R W. 1963. Evidence for genetic restriction of recombination in the lima bean. _Genetics_, 48, 1389–1395. CAS  PubMed  PubMed Central  Google Scholar  * Ayuzawa, CH, Sekodo, I,


Yamakawa, K, Sakukai, U, Kurata, W, Yaginuma, Y, and Tokoro, Y. 1972. _Handbook of Silkworm Rearing Agricultural Technique Manual_. Fuji Publishing Co. Ltd., Tokyo. Google Scholar  * De


Boer, R, and Van Der Hoeven, F A. 1977. Son-sire regression based on heritability estimates of chiasma frequency, using T7OH mouse translocation hctcrozygotes, and the relation between


univalence, chiasma frequency and sperm production. _Heredity_, 39, 335–343. Article  CAS  PubMed  Google Scholar  * Catcheside, D G. 1977. _The Genetics of Recombination_. Arnold, London.


Google Scholar  * Charlesworth, B, and Charlesworth, D. 1976. Theoretical genetics of Batesian mimicry. II. Evolution of supergenes. _J Theor Biol_, 55, 305–324. Article  Google Scholar  *


Chikushi, H. 1972. _Genes and Genetical Stocks of the Silkworm (Studies of Stock Culture in Biological Field No 1)_. Keigaku, Tokyo. Google Scholar  * Chinnici, J P. 1971a. Modification of


recombination frequency in Drosophila. I. Selection for increased and decreased crossing over. _Genetics_, 69, 71–83. CAS  PubMed  PubMed Central  Google Scholar  * Chinnici, J P. 1971b.


Modification of recombination frequency in Drosophila. II. The polygenic control of crossing over. _Genetics_, 69, 85–96. CAS  PubMed  PubMed Central  Google Scholar  * Clarke, C A, and


Sheppard, P M. 1971. Further studies on the genetics of the mimetic butterfly _Papilio memnon_ L. _Phil Trans Roy Soc London B_, 263, 35–70. Article  Google Scholar  * Clarke, C A, and


Sheppard, P M. 1972. The genetics of the mimetic butterfly _Popilio polytcs_ L. _Phil Trans Roy Soc London B_, 263, 431–458. Article  CAS  PubMed  Google Scholar  * Clarke, C A, and


Sheppard, P M. 1977. A new tailed female form of _Papilio memnon_ L. and its probable genetic control. _Syst Entomol_, 2, 17–19. Article  Google Scholar  * Clarke, C A, Sheppard, P M, and


Thornton, I W B. 1968. The genetics of the mimetic butterfly _Papilio memnon_ L. _Phil Trans Roy Soc London B_, 254, 37–89. Article  Google Scholar  * Dewees, A A. 1975. Genetic modification


of recombination rate in _Tribolium castaneum_. _Genetics_, 81, 537–552. CAS  PubMed  PubMed Central  Google Scholar  * Dryja, A. 1959. Badania nad polimorfizmem Kraśnika Zmiennego


(_Zygaena ephialtes_ L.). (Genetical investigation on the polymorphism of _Zygaena ephialtes_ L.). _Panstwowe Wydawnictwo Naukowe_, Warszawa, pp. 401 + folder of 12 plates and tables. *


Emsley, M G. 1965. The geographical distribution of the color-pattern components of _Heliconius erato_ and _Heliconius melpomcne_ with gcnctical evidence for the systematic relationship


between the two species. _Zoologica (New York)_, 49, 245–286. Google Scholar  * Fisher, R A. 1930. _The Gcnetical Theory of Natural Selection_. Clarendon Press, Oxford. Google Scholar  *


Hasimoto, H. 1960. Selection of crossover value between _Striped_ and _Yellow_ in the silkworm. _11ème Conference Technique Sericicole Internationale, Murcie (Espagne)_, 365–367. * Kidwell,


M G. 1972a. Genetic change of recombination value in _Drosophila melanogaster_. I. Artificial selection for high and low recombination and some properties of recombination-modifying genes.


_Genetics_, 70, 419–432. CAS  PubMed  PubMed Central  Google Scholar  * Kidwell, M G. 1972b. Genetic change of recombination value in _Drosophila melanogaster_. II. Simulated natural


selection. _Genetics_, 70, 433–443. CAS  PubMed  PubMed Central  Google Scholar  * Maynard Smith, J. 1977. Why the genome does not congeal. _Nature_, 268, 693–696. Article  Google Scholar  *


Maynard Smith, J. 1978. _The Evolution of Sex_. Cambridge University Press, London. Google Scholar  * Nei, M. 1969. Linkage modification and sex difference in recombination. _Genetics_, 63,


681–699. CAS  PubMed  PubMed Central  Google Scholar  * Parsons, P A. 1958. Selection for increased recombination in _Drosophila melanogaster_. _Amer Natur_, 92, 255–256. Article  Google


Scholar  * Schapp, T. 1978. Why should the genome congeal? _Nature_, 276, 535–536. Article  Google Scholar  * Shaw, D D. 1972. Genetic and environmental components of chiasma control. II.


The response to selection in _Schistocerca_. _Chromosoma_, 37, 297–308. Article  CAS  PubMed  Google Scholar  * Sheppard, P M. 1975. _Natural Selection and Heredity_, fourth edition.


Hutchinson, London. Google Scholar  * Sturtevant, A H. 1915. No crossing over in the female of the silkworm moth. _Amer Natur_, 49, 42–44. Article  Google Scholar  * Suomalainen, E. 1965. On


the chromosomes of the Geometrid moth genus _Cidaria_. _Chromosorna (Berlin)_, 16, 166–184. Article  Google Scholar  * Suomalainen, E, Cook, L H, and Turner, J R G. 1973. Achiasmatic


oogenesis in the heliconiine butterflies. _Hereditas_, 74, 302–304. Article  Google Scholar  * Traut, W. 1977. A study of recombination, formation of chiasmata and synaptonemal complexes in


female and male meiosis of _Ephestia kuehniella_ (Lepidoptera). _Genetica_, 47, 135–142. Article  Google Scholar  * Turner, J R G. 1971. Studies of Müllerian mimicry and its evolution in


burnet moths and heliconid butterflies. In _Ecological Genetics and Evolution_, ed. E. R. Creed, pp. 224–260. Blackwell Scientific Publications, Oxford. Chapter  Google Scholar  * Turner, J


R G. 1975. A tale of two butterflies. _Natural History_, 84 (2), 28–37. Google Scholar  * Turner, J R G. 1976. Muellerian mimicry: classical “beanbag” evolution, and the role of ecological


islands in adaptive race formation. In _Population Genetics and Ecology_, ed. S. Karlin and E. Nevo, pp. 185–218. Academic Press, New York and London. Google Scholar  * Turner, J R G. 1977.


Butterfly mimicry: the genetical evolution of an adaptation. _Evol Biol_, 10, 163–206. Google Scholar  * Turner, J R G, and Crane, J. 1962. The genetics of some polymorphic forms of the


butterflies _Heliconius melpomene_ Linnaeus and _H. erato_ Linnaeus. I. Major genes. _Zoologica (New York)_, 47, 141–152. Google Scholar  * Turner, J R G, Johnson, M S, and Eanes, W F. 1979.


Contrasted modes of evolution in the same genome: allozymes and adaptive change in _Heliconius_. _Proc Natl Acad Sci USA_, 76, 1924–1928. Article  CAS  PubMed  PubMed Central  Google


Scholar  * Turner, J R G, and Sheppard, P M. 1975. Absence of crossing-over in female butterflies (_Heliconius_). _Heredity_, 34, 265–269. Article  PubMed  Google Scholar  Download


references ACKNOWLEDGEMENTS Acknowledgments.-The progress of this work has been dependent on the considerable skills of Mr Mart Koello, who adapted the Japanese techniques of silkworm


rearing to our needs, and oversaw the rearing of the broods ; he is co-author of section 3. Much additional help was provided by Dr Charles Mitter, Mr Craig Sargent and Ms Melody Wolstoff.


To all these people I am extremely grateful. I am much indebted to Professor Hiroshi Doira who provided several batches of the high and low stocks from Kyushu University. The research was


supported by grant 5 ROI GM 20702 from the National Institutes of Health. AUTHOR INFORMATION Author notes * John R G Turner Present address: Department of Genetics, University of Leeds,


Leeds, LS2 9JT, England AUTHORS AND AFFILIATIONS * Department of Ecology and Evolution, State University of New York, Stony Brook, 11794, N.Y., USA John R G Turner Authors * John R G Turner


View author publications You can also search for this author inPubMed Google Scholar ADDITIONAL INFORMATION Contribution number 318 from the Program in Ecology and Evolution of the State


University of New York at Stony Brook. RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Turner, J. Genetic control of recombination in the silkworm.


_Heredity_ 43, 273–293 (1979). https://doi.org/10.1038/hdy.1979.83 Download citation * Received: 26 March 1979 * Issue Date: 01 October 1979 * DOI: https://doi.org/10.1038/hdy.1979.83 SHARE


THIS ARTICLE Anyone you share the following link with will be able to read this content: Get shareable link Sorry, a shareable link is not currently available for this article. Copy to


clipboard Provided by the Springer Nature SharedIt content-sharing initiative