Divergent evolution of male-determining loci on proto-Y chromosomes of the housefly

Xuan Li; Sander Visser; Jae Hak Son; Elzemiek Geuverink; Ece Naz Kıvanç; Yanli Wu; Stephan Schmeing; Martin Pippel; Seyed Yahya Anvar; Martijn A. Schenkel; František Marec; Mark D. Robinson; Richard P. Meisel; Ernst A. Wimmer; Louis van de Zande; Daniel Bopp; Leo W. Beukeboom

doi:10.1038/s41467-024-50390-1

Divergent evolution of male-determining loci on proto-Y chromosomes of the housefly

Xuan Li^*, Sander Visser, Jae Hak Son, Elzemiek Geuverink, Ece Naz Kıvanç, Yanli Wu, Stephan Schmeing, Martin Pippel, Seyed Yahya Anvar, Martijn A. Schenkel, František Marec, Mark D. Robinson, Richard P. Meisel, Ernst A. Wimmer, Louis van de Zande, Daniel Bopp, Leo W. Beukeboom

^*Corresponding author for this work

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Abstract

Houseflies provide a good experimental model to study the initial evolutionary stages of a primary sex-determining locus because they possess different recently evolved proto-Y chromosomes that contain male-determining loci (M) with the same male-determining gene, Mdmd. We investigate M-loci genomically and cytogenetically revealing distinct molecular architectures among M-loci. M on chromosome V (M^V) has two intact Mdmd copies in a palindrome. M on chromosome III (M^III) has tandem duplications containing 88 Mdmd copies (only one intact) and various repeats, including repeats that are XY-prevalent. M on chromosome II (M^II) and the Y (M^Y) share M^III-like architecture, but with fewer repeats. M^Y additionally shares M^V-specific sequence arrangements. Based on these data and karyograms using two probes, one derives from M^III and one Mdmd-specific, we infer evolutionary histories of polymorphic M-loci, which have arisen from unique translocations of Mdmd, embedded in larger DNA fragments, and diverged independently into regions of varying complexity.

Original language	English
Article number	5984
Number of pages	13
Journal	Nature Communications
Volume	15
Issue number	1
DOIs	https://doi.org/10.1038/s41467-024-50390-1
Publication status	Published - Dec-2024

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Divergent evolution of male-determining loci on proto-Y chromosomes of the houseflyFinal publisher's version, 1.77 MBLicence: CC BY

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Li, X., Visser, S., Son, J. H., Geuverink, E., Kıvanç, E. N., Wu, Y., Schmeing, S., Pippel, M., Anvar, S. Y., Schenkel, M. A., Marec, F., Robinson, M. D., Meisel, R. P., Wimmer, E. A., van de Zande, L., Bopp, D., & Beukeboom, L. W. (2024). Divergent evolution of male-determining loci on proto-Y chromosomes of the housefly. Nature Communications, 15(1), Article 5984. https://doi.org/10.1038/s41467-024-50390-1

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title = "Divergent evolution of male-determining loci on proto-Y chromosomes of the housefly",

abstract = "Houseflies provide a good experimental model to study the initial evolutionary stages of a primary sex-determining locus because they possess different recently evolved proto-Y chromosomes that contain male-determining loci (M) with the same male-determining gene, Mdmd. We investigate M-loci genomically and cytogenetically revealing distinct molecular architectures among M-loci. M on chromosome V (MV) has two intact Mdmd copies in a palindrome. M on chromosome III (MIII) has tandem duplications containing 88 Mdmd copies (only one intact) and various repeats, including repeats that are XY-prevalent. M on chromosome II (MII) and the Y (MY) share MIII-like architecture, but with fewer repeats. MY additionally shares MV-specific sequence arrangements. Based on these data and karyograms using two probes, one derives from MIII and one Mdmd-specific, we infer evolutionary histories of polymorphic M-loci, which have arisen from unique translocations of Mdmd, embedded in larger DNA fragments, and diverged independently into regions of varying complexity.",

author = "Xuan Li and Sander Visser and Son, {Jae Hak} and Elzemiek Geuverink and Kıvan{\c c}, {Ece Naz} and Yanli Wu and Stephan Schmeing and Martin Pippel and Anvar, {Seyed Yahya} and Schenkel, {Martijn A.} and Franti{\v s}ek Marec and Robinson, {Mark D.} and Meisel, {Richard P.} and Wimmer, {Ernst A.} and {van de Zande}, Louis and Daniel Bopp and Beukeboom, {Leo W.}",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2024",

month = dec,

doi = "10.1038/s41467-024-50390-1",

language = "English",

volume = "15",

journal = "Nature Communications",

issn = "2041-1723",

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Li, X, Visser, S, Son, JH, Geuverink, E, Kıvanç, EN, Wu, Y, Schmeing, S, Pippel, M, Anvar, SY, Schenkel, MA, Marec, F, Robinson, MD, Meisel, RP, Wimmer, EA, van de Zande, L, Bopp, D & Beukeboom, LW 2024, 'Divergent evolution of male-determining loci on proto-Y chromosomes of the housefly', Nature Communications, vol. 15, no. 1, 5984. https://doi.org/10.1038/s41467-024-50390-1

TY - JOUR

T1 - Divergent evolution of male-determining loci on proto-Y chromosomes of the housefly

AU - Li, Xuan

AU - Visser, Sander

AU - Son, Jae Hak

AU - Geuverink, Elzemiek

AU - Kıvanç, Ece Naz

AU - Wu, Yanli

AU - Schmeing, Stephan

AU - Pippel, Martin

AU - Anvar, Seyed Yahya

AU - Schenkel, Martijn A.

AU - Marec, František

AU - Robinson, Mark D.

AU - Meisel, Richard P.

AU - Wimmer, Ernst A.

AU - van de Zande, Louis

AU - Bopp, Daniel

AU - Beukeboom, Leo W.

PY - 2024/12

Y1 - 2024/12

N2 - Houseflies provide a good experimental model to study the initial evolutionary stages of a primary sex-determining locus because they possess different recently evolved proto-Y chromosomes that contain male-determining loci (M) with the same male-determining gene, Mdmd. We investigate M-loci genomically and cytogenetically revealing distinct molecular architectures among M-loci. M on chromosome V (MV) has two intact Mdmd copies in a palindrome. M on chromosome III (MIII) has tandem duplications containing 88 Mdmd copies (only one intact) and various repeats, including repeats that are XY-prevalent. M on chromosome II (MII) and the Y (MY) share MIII-like architecture, but with fewer repeats. MY additionally shares MV-specific sequence arrangements. Based on these data and karyograms using two probes, one derives from MIII and one Mdmd-specific, we infer evolutionary histories of polymorphic M-loci, which have arisen from unique translocations of Mdmd, embedded in larger DNA fragments, and diverged independently into regions of varying complexity.

AB - Houseflies provide a good experimental model to study the initial evolutionary stages of a primary sex-determining locus because they possess different recently evolved proto-Y chromosomes that contain male-determining loci (M) with the same male-determining gene, Mdmd. We investigate M-loci genomically and cytogenetically revealing distinct molecular architectures among M-loci. M on chromosome V (MV) has two intact Mdmd copies in a palindrome. M on chromosome III (MIII) has tandem duplications containing 88 Mdmd copies (only one intact) and various repeats, including repeats that are XY-prevalent. M on chromosome II (MII) and the Y (MY) share MIII-like architecture, but with fewer repeats. MY additionally shares MV-specific sequence arrangements. Based on these data and karyograms using two probes, one derives from MIII and one Mdmd-specific, we infer evolutionary histories of polymorphic M-loci, which have arisen from unique translocations of Mdmd, embedded in larger DNA fragments, and diverged independently into regions of varying complexity.

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DO - 10.1038/s41467-024-50390-1

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AN - SCOPUS:85198738522

SN - 2041-1723

VL - 15

JO - Nature Communications

JF - Nature Communications

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ER -

Divergent evolution of male-determining loci on proto-Y chromosomes of the housefly

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