Recombination Suppression Drives Expansion of the <i>Drosophila</i> Dot Chromosome

Genome size varies widely, even among closely related species, yet much less is known about chromosome size variation. Here we use the fourth chromosome of Drosophila, also known as the "Muller F element" or "dot chromosome", as a model to investigate chromosome-specific size expansion. The F element of most Drosophila species is small (∼1.3 Mb) and almost entirely heterochromatic, yet harbors approximately 80 protein-coding genes. Here, we study D. kikkawai, D. takahashii, D. ananassae, and D. bipectinata, whose F elements are 2- to 15-fold larger in size compared to D. melanogaster. Through manual gene curation and comparative genomic analysis, we find that their F elements have expanded primarily via accumulation of transposable elements (TEs) in introns and intergenic regions. Natural selection appears less efficient on these expanded F elements: they have smaller effective population sizes and their genes exhibit reduced usage of optimal codons, compared to D. melanogaster. We propose that F element size variation is driven by differences in F element recombination rates. The ultra-long (∼20 Mb) F elements of D. ananassae and D. bipectinata display high rates of rearrangement and sequence evolution and exhibit independent TE-driven expansions. Our results suggest that F elements of most Drosophila species likely recombine enough to prevent size expansion, while F element recombination in D. ananassae and D. bipectinata is either absent or rare enough to allow TEs and other deleterious mutations to accumulate via Muller's ratchet; thus, these chromosomes evolve more like a Y chromosome than a typical Drosophila F element.

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Journal
Molecular Biology and Evolution
Published
2025-11-28
DOI
https://doi.org/10.1093/molbev/msaf304
Primary Topic
Chromosomal and Genetic Variations
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article
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article

Recombination Suppression Drives Expansion of the Drosophila Dot Chromosome

Melanie M. Reynoso, Sheel Singh, Jade Enright, William D Gilliland et al.
Molecular Biology and Evolution
Chromosomal and Genetic Variations
article

Recombination Suppression Drives Expansion of the Drosophila Dot Chromosome

Melanie M. Reynoso, Sheel Singh, Jade Enright, William D Gilliland, Jacklyn Thomas, Paige A. LaMore, Daija Dennis, Ethan Cordes, Evan N. Bennett, Michaël Tran, Isabelle St-Martin, Aishah Kothawala, Sarah A. Peck Justice, Alice Herrmann, Kelly Hartigan, Caroline Lutz, Lauren E. Bahr, Jordan E. Odell, Andrea Pietruska, Victoria Ramage, Caleb Rhyne, Howard Granok, Dakota Ellis, Samantha L. Zimmerman, Jasmine Roman, C. Shaffer, Jason Barrios, Samuel R. Alper, Andrew M. Arsham, Leah Frederick, Alicia N. Wilkening, Molly Charney, Paula Croonquist, Sahil Chandhok, Graham Bachman, Cindy S. Malone, Charles R. Hauser, E. Oh, Den Lipata, Amy Kwan, Stephen Daly, Cindy Arrigo, J. Cuñé Sala, Haolin Shen, Andrew Galley, D. Harper, Abigail A. Ruiz, Ashley Erickson, Mohammad Sujaur Rahman, Dennis Revie, John M. Braverman, Sara Spells, Thomas C. Giarla, Melanie Van Stry, Cassidy Schneider, Manasvi Verma, Tia B. Watkins, Brooke Felsheim, Susan Parrish, Mary Ellen Conley, Ashly Nsangou, Norma Velazquez-Ulloa, Sukruth Amogh Shashikumar, M. Chamberlain, Maria Santisteban, Jack E. Frierson, Alma Rodriguez Estrada, Alondra M. Diaz Lameiro, Lauren D. Gann, Conor McCarthy, Alexandra LaFollette, Emmaline Prinz, Michael S. Foulk, Ibrahim Khandakar, Julie Sauvageau, Amanda Moy, Carina E. Howell, Janae Marie. Hughes, Jennifer A. Kennell, Jennifer C. Jemc, Audrey Widmier, Luis Alcantar, Troy LoBue, Kaila Gemenes, Siaumin Fung, Nicole Sam, Jamie Siders, Ashitha Dama, Christopher E. Ellison, Jasdeep Dhahan, Taylor Coffman, Julie M. Starkey, Sujung Crystal Shin, Joyce Ruan, Teagan Thomas, Avril Alfred, Elizabeth Huntington, Lana Tinawi, Leah Paul, William H. Goo, Ken Saville, Juliana Choza, Sophia L TumSuden, Chioma Okuagu, Briana N Felix, Adam T. Smiley, Timothy J. Stanek, Purui Xu, Dinah Arafeh, Eleanor I. Sams, Rebecca Spokony, E Woodward, Caroline Ugoaru, Chandler Bradford, Katheryn P. Franklin, Leocadia V. Paliulis, Judith L. Leatherman, Nicole S. Torosin, Muhammad G. Mousa, Priyali Patel, Viviana Domínguez, Kaylah B. Samuelson, Alejandro Arriaga, Brooke Gillis, Zachary T. Sentell, Matthew R. Skerritt, Krithika Mohan, Elizabeth M. Miller, Regina Ball, Jose Lizarraga Mazaba, James S. Godde, Cooper Hostetler, Paige K. Thompson, Dawn Zapata, Sophia Valenti, Keith Schreiber, Stephanie Toering Peters, Hacina Gill, Melissa McCarter, Terry Letsche, Katie Goodenow, Alexander Gažo, Markcus Lee, Zachery J. Deckner, Garrett D. Chavis, Andrew J. Tonsager, Wilson Leung, Evan Merkhofer, Jim Youngblom, 義夫 田中, Amy T. Hark, Kaitlyn Stroscio, Amie J. McClellan, Katie L. Holland, Joshua Hughes, Eryn Braley, Rebecca Hatcher, Alexis Godfrey, Stephen M. Tansie, Srebrenka Robic, Pouria Asadi, Amari Michaux, Lisa Kadlec, Harshal Mehta, Jessie Gallo, Laurie S. Stevison, Tamara L. Mans, Leslie E. Green Pimentel, Brianna Femenella, Lauren E. 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Croucher, Sanjeevani Bhavsar, Nnamdi Nwoke, Bethany D. Bengs, Amo Ikiror, Sabrina Ramos, Comfort Y. Adegboye, Victoria R. Miduri, Rosario C Lopez-Roca Fernandez, Simran Shrestha, Thao Thanh Huynh, Trina L. Chou, Sarah Kelly, Trinh Tran, Jordan M. Kintigh, Laura K Reed, Joyi Wong, Sahar Anis Ali, Angel Nichols, Zachary Peters Wakefield, Joshua Thorpe, Natalie Graff, Jake Holechek, Mia Mo, Gaelle Umutoni Mihigo, Bailee D. Werner, Jason Rettger, Marlene Hernandez, Kaylyn Rowsey, Jordan Myers, Lisa Evans, Ezra Belay, William Morris, Amy Jones, Lauren Wells, M. Grigg, Jordyn Britton, Rhiannon E. Jones, Shu Liao, Indrani Bose, Jupiter C. Kalinowski, Justin Patino, Jenna M. Peterson, Leming Zhou, Laura Santander Diaz, ASHLEY NGUYEN, H. Sato, A. B. J. Clark, CHRIS MCCURRY, Martin G. Burg, Emily Ruth Sartori, B. W. Griffiths, Sydney Elder, Casey Hannah, Gregory Sileo, Sam Ranger, Destiny Sabb, Kacie Kershaw, Cameron Welles, Joshua Kurucz, Faith J. Boyer-Millander, Christopher Hemauer, Chirayu Salgarkar, Dakota Wilkinson, Nelson Catherine, Bryan C. Armpriest, Oswaldo L. Echevarría-Bonilla, Dominic Duke Quattrochi, Haleigh C Wooters, Eman Khan, Mariana González-Aguilar, Maëlle T. Gace, Vanessa Tuytel, Jaely Z. Chavez, Bianca Kyrie Wanamaker, Benjamin Galligos, Isabella Peetz, Cody Fondse, Taysia Nikaido-Landry, Sara J Davila Severiano, Sarah C R Elgin, Nhi N T Vuong, Emily K Sayre, The Genomics Education Partnership, Ritij Sarvaiya, Mitzy G Dominguez-Vera, Jessica Daveshar, Alia Botan, Joseph J Hobbie, Juan Carlos Martínez-Cruzado, Jacqueline L Barry, Tegvir Dhanoa, Savannah Alvarez, Elynna B Youm, Yuliya Mazo, Mayra Alcaraz-Lopez, Lisa Nagar, Ryan J Wanless, Emily Kedziorek, Mark W Gonzalez, Robyn Huber, Meghna Pandey, Francesca Danielle Rasmus, Diego Enrique Flores Ayala, Peyton Taylor Fair, Emily M Marticello, Alyssa Peeples, Amar Karahodzic, Lyeng Lim, Anisa Vakalia, Emma V Danylin, Harrison A B Sanger, Alisha Bajracharya, Sebastian Jaramillo, Ethan S Presgrove, Su Ji Kim, Ashley N Penalbert, Megan Parenteau, Megan Ritter, Molly Key, Morgan E Bishop, Haroon Qureshi, Jalynn M Ledford, Jaquelyn Hester, Angelique Wooley, Tyler S Passmore, Ali Lenard, Marielle Parks, Howard N Rainey, Kleamcy 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Destiny-Rose Chery, LaKaiya C Campbell, Minh-Sang Lu, Jay A Patel, Dakota Cao, Theron Gunderson, Anna K Allen, Julia L Tangorra, Trevor R Johnson, Megan R Lewis-Kiddie, Payton Jamieson, Sara Ochterski, Liza V Jiménez-Rodríguez, Angela Beyler, Kyung Joo Son, Makenzie Ryan, Amari Pickett, Rachael R Dioguardi, Nathaniel Wiggley, Alison Bakowski, Daniel R Ramirez, Adilene Ambriz, Jessalyn Nguyen, Drew Tonsager, Jenna R Cavalieri, Ebony V Chilin, Jack Carter, Sergiu-Mihai Ciavoi, Wesley A Miller, Arthi Shankar, Priscilla M Gonzalez, Amaya E Rogers, Dang H Vu, Yordanos S Belachew, Gates Leonard, Madeleine Green, Meghan E Nasman, Daniela L Barragan, José A Chaparro Galloza, Lillian Duce, Aspen B Chadderdon, Helena Santiana, MaryAnn R Conklin, Lauren McEntyre, Sutton C Kemp, Louis Connelly
article en

Abstract

Genome size varies widely, even among closely related species, yet much less is known about chromosome size variation. Here we use the fourth chromosome of Drosophila, also known as the "Muller F element" or "dot chromosome", as a model to investigate chromosome-specific size expansion. The F element of most Drosophila species is small (∼1.3 Mb) and almost entirely heterochromatic, yet harbors approximately 80 protein-coding genes. Here, we study D. kikkawai, D. takahashii, D. ananassae, and D. bipectinata, whose F elements are 2- to 15-fold larger in size compared to D. melanogaster. Through manual gene curation and comparative genomic analysis, we find that their F elements have expanded primarily via accumulation of transposable elements (TEs) in introns and intergenic regions. Natural selection appears less efficient on these expanded F elements: they have smaller effective population sizes and their genes exhibit reduced usage of optimal codons, compared to D. melanogaster. We propose that F element size variation is driven by differences in F element recombination rates. The ultra-long (∼20 Mb) F elements of D. ananassae and D. bipectinata display high rates of rearrangement and sequence evolution and exhibit independent TE-driven expansions. Our results suggest that F elements of most Drosophila species likely recombine enough to prevent size expansion, while F element recombination in D. ananassae and D. bipectinata is either absent or rare enough to allow TEs and other deleterious mutations to accumulate via Muller's ratchet; thus, these chromosomes evolve more like a Y chromosome than a typical Drosophila F element.

Molecular Biology and EvolutionVol. 42(12)
University of Alabama (US), Washington University in St. Louis (US), Environmental and Occupational Health Sciences Institute (US), Institute of Human Genetics (PL), Saint Joseph's University (US), Lewis & Clark College (US), New Jersey City University (US)
National Science Foundation, Rutgers, The State University of New Jersey, National Institutes of Health, Office of Advanced Research Computing, Rutgers, The State University of New Jersey
Openalex Percentile: Top 24%
Chromosomal and Genetic Variations
DOIOpen Access PDFOpenAlex
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