Sequence analysis in Bos taurus reveals pervasiveness of X–Y arms races in mammalian lineages
© 2020 Hughes et al. Studies of Y Chromosome evolution have focused primarily on gene decay, a consequence of suppression of crossing-over with the X Chromosome. Here, we provide evidence that suppression of X–Y crossing-over unleashed a second dynamic: selfish X–Y arms races that reshaped the sex c...
| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Cold Spring Harbor Laboratory
2021
|
| Online Access: | https://hdl.handle.net/1721.1/134379 |
| _version_ | 1826215894114631680 |
|---|---|
| author | Hughes, Jennifer F Skaletsky, Helen Pyntikova, Tatyana Koutseva, Natalia Raudsepp, Terje Brown, Laura G Bellott, Daniel W Cho, Ting-Jan Dugan-Rocha, Shannon Khan, Ziad Kremitzki, Colin Fronick, Catrina Graves-Lindsay, Tina A Fulton, Lucinda Warren, Wesley C Wilson, Richard K Owens, Elaine Womack, James E Murphy, William J Muzny, Donna M Worley, Kim C Chowdhary, Bhanu P Gibbs, Richard A Page, David C |
| author_facet | Hughes, Jennifer F Skaletsky, Helen Pyntikova, Tatyana Koutseva, Natalia Raudsepp, Terje Brown, Laura G Bellott, Daniel W Cho, Ting-Jan Dugan-Rocha, Shannon Khan, Ziad Kremitzki, Colin Fronick, Catrina Graves-Lindsay, Tina A Fulton, Lucinda Warren, Wesley C Wilson, Richard K Owens, Elaine Womack, James E Murphy, William J Muzny, Donna M Worley, Kim C Chowdhary, Bhanu P Gibbs, Richard A Page, David C |
| author_sort | Hughes, Jennifer F |
| collection | MIT |
| description | © 2020 Hughes et al. Studies of Y Chromosome evolution have focused primarily on gene decay, a consequence of suppression of crossing-over with the X Chromosome. Here, we provide evidence that suppression of X–Y crossing-over unleashed a second dynamic: selfish X–Y arms races that reshaped the sex chromosomes in mammals as different as cattle, mice, and men. Using super-resolution sequencing, we explore the Y Chromosome of Bos taurus (bull) and find it to be dominated by massive, lineage-specific amplification of testis-expressed gene families, making it the most gene-dense Y Chromosome sequenced to date. As in mice, an X-linked homolog of a bull Y-amplified gene has become testis-specific and amplified. This evolutionary convergence implies that lineage-specific X–Y coevolution through gene amplification, and the selfish forces underlying this phenomenon, were dominatingly powerful among diverse mammalian lineages. Together with Y gene decay, X–Y arms races molded mammalian sex chromosomes and influenced the course of mammalian evolution. |
| first_indexed | 2024-09-23T16:38:43Z |
| format | Article |
| id | mit-1721.1/134379 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T16:38:43Z |
| publishDate | 2021 |
| publisher | Cold Spring Harbor Laboratory |
| record_format | dspace |
| spelling | mit-1721.1/1343792021-10-28T03:08:27Z Sequence analysis in Bos taurus reveals pervasiveness of X–Y arms races in mammalian lineages Hughes, Jennifer F Skaletsky, Helen Pyntikova, Tatyana Koutseva, Natalia Raudsepp, Terje Brown, Laura G Bellott, Daniel W Cho, Ting-Jan Dugan-Rocha, Shannon Khan, Ziad Kremitzki, Colin Fronick, Catrina Graves-Lindsay, Tina A Fulton, Lucinda Warren, Wesley C Wilson, Richard K Owens, Elaine Womack, James E Murphy, William J Muzny, Donna M Worley, Kim C Chowdhary, Bhanu P Gibbs, Richard A Page, David C © 2020 Hughes et al. Studies of Y Chromosome evolution have focused primarily on gene decay, a consequence of suppression of crossing-over with the X Chromosome. Here, we provide evidence that suppression of X–Y crossing-over unleashed a second dynamic: selfish X–Y arms races that reshaped the sex chromosomes in mammals as different as cattle, mice, and men. Using super-resolution sequencing, we explore the Y Chromosome of Bos taurus (bull) and find it to be dominated by massive, lineage-specific amplification of testis-expressed gene families, making it the most gene-dense Y Chromosome sequenced to date. As in mice, an X-linked homolog of a bull Y-amplified gene has become testis-specific and amplified. This evolutionary convergence implies that lineage-specific X–Y coevolution through gene amplification, and the selfish forces underlying this phenomenon, were dominatingly powerful among diverse mammalian lineages. Together with Y gene decay, X–Y arms races molded mammalian sex chromosomes and influenced the course of mammalian evolution. 2021-10-27T20:04:43Z 2021-10-27T20:04:43Z 2020 2021-07-21T17:48:04Z Article http://purl.org/eprint/type/JournalArticle https://hdl.handle.net/1721.1/134379 en 10.1101/gr.269902.120 Genome Research Creative Commons Attribution NonCommercial License 4.0 https://creativecommons.org/licenses/by-nc/4.0/ application/pdf Cold Spring Harbor Laboratory Cold Spring Harbor Laboratory Press |
| spellingShingle | Hughes, Jennifer F Skaletsky, Helen Pyntikova, Tatyana Koutseva, Natalia Raudsepp, Terje Brown, Laura G Bellott, Daniel W Cho, Ting-Jan Dugan-Rocha, Shannon Khan, Ziad Kremitzki, Colin Fronick, Catrina Graves-Lindsay, Tina A Fulton, Lucinda Warren, Wesley C Wilson, Richard K Owens, Elaine Womack, James E Murphy, William J Muzny, Donna M Worley, Kim C Chowdhary, Bhanu P Gibbs, Richard A Page, David C Sequence analysis in Bos taurus reveals pervasiveness of X–Y arms races in mammalian lineages |
| title | Sequence analysis in Bos taurus reveals pervasiveness of X–Y arms races in mammalian lineages |
| title_full | Sequence analysis in Bos taurus reveals pervasiveness of X–Y arms races in mammalian lineages |
| title_fullStr | Sequence analysis in Bos taurus reveals pervasiveness of X–Y arms races in mammalian lineages |
| title_full_unstemmed | Sequence analysis in Bos taurus reveals pervasiveness of X–Y arms races in mammalian lineages |
| title_short | Sequence analysis in Bos taurus reveals pervasiveness of X–Y arms races in mammalian lineages |
| title_sort | sequence analysis in bos taurus reveals pervasiveness of x y arms races in mammalian lineages |
| url | https://hdl.handle.net/1721.1/134379 |
| work_keys_str_mv | AT hughesjenniferf sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT skaletskyhelen sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT pyntikovatatyana sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT koutsevanatalia sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT raudseppterje sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT brownlaurag sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT bellottdanielw sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT chotingjan sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT duganrochashannon sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT khanziad sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT kremitzkicolin sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT fronickcatrina sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT graveslindsaytinaa sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT fultonlucinda sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT warrenwesleyc sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT wilsonrichardk sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT owenselaine sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT womackjamese sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT murphywilliamj sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT muznydonnam sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT worleykimc sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT chowdharybhanup sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT gibbsricharda sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages AT pagedavidc sequenceanalysisinbostaurusrevealspervasivenessofxyarmsracesinmammalianlineages |