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Drosophila muller f elements maintain a distinct set of genomic properties over 40 million years of evolution.

  • Author(s): Leung, Wilson;
  • Shaffer, Christopher D;
  • Reed, Laura K;
  • Smith, Sheryl T;
  • Barshop, William;
  • Dirkes, William;
  • Dothager, Matthew;
  • Lee, Paul;
  • Wong, Jeannette;
  • Xiong, David;
  • Yuan, Han;
  • Bedard, James EJ;
  • Machone, Joshua F;
  • Patterson, Seantay D;
  • Price, Amber L;
  • Turner, Bryce A;
  • Robic, Srebrenka;
  • Luippold, Erin K;
  • McCartha, Shannon R;
  • Walji, Tezin A;
  • Walker, Chelsea A;
  • Saville, Kenneth;
  • Abrams, Marita K;
  • Armstrong, Andrew R;
  • Armstrong, William;
  • Bailey, Robert J;
  • Barberi, Chelsea R;
  • Beck, Lauren R;
  • Blaker, Amanda L;
  • Blunden, Christopher E;
  • Brand, Jordan P;
  • Brock, Ethan J;
  • Brooks, Dana W;
  • Brown, Marie;
  • Butzler, Sarah C;
  • Clark, Eric M;
  • Clark, Nicole B;
  • Collins, Ashley A;
  • Cotteleer, Rebecca J;
  • Cullimore, Peterson R;
  • Dawson, Seth G;
  • Docking, Carter T;
  • Dorsett, Sasha L;
  • Dougherty, Grace A;
  • Downey, Kaitlyn A;
  • Drake, Andrew P;
  • Earl, Erica K;
  • Floyd, Trevor G;
  • Forsyth, Joshua D;
  • Foust, Jonathan D;
  • Franchi, Spencer L;
  • Geary, James F;
  • Hanson, Cynthia K;
  • Harding, Taylor S;
  • Harris, Cameron B;
  • Heckman, Jonathan M;
  • Holderness, Heather L;
  • Howey, Nicole A;
  • Jacobs, Dontae A;
  • Jewell, Elizabeth S;
  • Kaisler, Maria;
  • Karaska, Elizabeth A;
  • Kehoe, James L;
  • Koaches, Hannah C;
  • Koehler, Jessica;
  • Koenig, Dana;
  • Kujawski, Alexander J;
  • Kus, Jordan E;
  • Lammers, Jennifer A;
  • Leads, Rachel R;
  • Leatherman, Emily C;
  • Lippert, Rachel N;
  • Messenger, Gregory S;
  • Morrow, Adam T;
  • Newcomb, Victoria;
  • Plasman, Haley J;
  • Potocny, Stephanie J;
  • Powers, Michelle K;
  • Reem, Rachel M;
  • Rennhack, Jonathan P;
  • Reynolds, Katherine R;
  • Reynolds, Lyndsey A;
  • Rhee, Dong K;
  • Rivard, Allyson B;
  • Ronk, Adam J;
  • Rooney, Meghan B;
  • Rubin, Lainey S;
  • Salbert, Luke R;
  • Saluja, Rasleen K;
  • Schauder, Taylor;
  • Schneiter, Allison R;
  • Schulz, Robert W;
  • Smith, Karl E;
  • Spencer, Sarah;
  • Swanson, Bryant R;
  • Tache, Melissa A;
  • Tewilliager, Ashley A;
  • Tilot, Amanda K;
  • VanEck, Eve;
  • Villerot, Matthew M;
  • Vylonis, Megan B;
  • Watson, David T;
  • Wurzler, Juliana A;
  • Wysocki, Lauren M;
  • Yalamanchili, Monica;
  • Zaborowicz, Matthew A;
  • Emerson, Julia A;
  • Ortiz, Carlos;
  • Deuschle, Frederic J;
  • DiLorenzo, Lauren A;
  • Goeller, Katie L;
  • Macchi, Christopher R;
  • Muller, Sarah E;
  • Pasierb, Brittany D;
  • Sable, Joseph E;
  • Tucci, Jessica M;
  • Tynon, Marykathryn;
  • Dunbar, David A;
  • Beken, Levent H;
  • Conturso, Alaina C;
  • Danner, Benjamin L;
  • DeMichele, Gabriella A;
  • Gonzales, Justin A;
  • Hammond, Maureen S;
  • Kelley, Colleen V;
  • Kelly, Elisabeth A;
  • Kulich, Danielle;
  • Mageeney, Catherine M;
  • McCabe, Nikie L;
  • Newman, Alyssa M;
  • Spaeder, Lindsay A;
  • Tumminello, Richard A;
  • Revie, Dennis;
  • Benson, Jonathon M;
  • Cristostomo, Michael C;
  • DaSilva, Paolo A;
  • Harker, Katherine S;
  • Jarrell, Jenifer N;
  • Jimenez, Luis A;
  • Katz, Brandon M;
  • Kennedy, William R;
  • Kolibas, Kimberly S;
  • LeBlanc, Mark T;
  • Nguyen, Trung T;
  • Nicolas, Daniel S;
  • Patao, Melissa D;
  • Patao, Shane M;
  • Rupley, Bryan J;
  • Sessions, Bridget J;
  • Weaver, Jennifer A;
  • Goodman, Anya L;
  • Alvendia, Erica L;
  • Baldassari, Shana M;
  • Brown, Ashley S;
  • Chase, Ian O;
  • Chen, Maida;
  • Chiang, Scott;
  • Cromwell, Avery B;
  • Custer, Ashley F;
  • DiTommaso, Tia M;
  • El-Adaimi, Jad;
  • Goscinski, Nora C;
  • Grove, Ryan A;
  • Gutierrez, Nestor;
  • Harnoto, Raechel S;
  • Hedeen, Heather;
  • Hong, Emily L;
  • Hopkins, Barbara L;
  • Huerta, Vilma F;
  • Khoshabian, Colin;
  • LaForge, Kristin M;
  • Lee, Cassidy T;
  • Lewis, Benjamin M;
  • Lydon, Anniken M;
  • Maniaci, Brian J;
  • Mitchell, Ryan D;
  • Morlock, Elaine V;
  • Morris, William M;
  • Naik, Priyanka;
  • Olson, Nicole C;
  • Osterloh, Jeannette M;
  • Perez, Marcos A;
  • Presley, Jonathan D;
  • Randazzo, Matt J;
  • Regan, Melanie K;
  • Rossi, Franca G;
  • Smith, Melanie A;
  • Soliterman, Eugenia A;
  • Sparks, Ciani J;
  • Tran, Danny L;
  • Wan, Tiffany;
  • Welker, Anne A;
  • Wong, Jeremy N;
  • Sreenivasan, Aparna;
  • Youngblom, Jim;
  • Adams, Andrew;
  • Alldredge, Justin;
  • Bryant, Ashley;
  • Carranza, David;
  • Cifelli, Alyssa;
  • Coulson, Kevin;
  • Debow, Calise;
  • Delacruz, Noelle;
  • Emerson, Charlene;
  • Farrar, Cassandra;
  • Foret, Don;
  • Garibay, Edgar;
  • Gooch, John;
  • Heslop, Michelle;
  • Kaur, Sukhjit;
  • Khan, Ambreen;
  • Kim, Van;
  • Lamb, Travis;
  • Lindbeck, Peter;
  • Lucas, Gabi;
  • Macias, Elizabeth;
  • Martiniuc, Daniela;
  • Mayorga, Lissett;
  • Medina, Joseph;
  • Membreno, Nelson;
  • Messiah, Shady;
  • Neufeld, Lacey;
  • Nguyen, San Francisco;
  • Nichols, Zachary;
  • Odisho, George;
  • Peterson, Daymon;
  • Rodela, Laura;
  • Rodriguez, Priscilla;
  • Rodriguez, Vanessa;
  • Ruiz, Jorge;
  • Sherrill, Will;
  • Silva, Valeria;
  • Sparks, Jeri;
  • Statton, Geeta;
  • Townsend, Ashley;
  • Valdez, Isabel;
  • Waters, Mary;
  • Westphal, Kyle;
  • Winkler, Stacey;
  • Zumkehr, Joannee;
  • DeJong, Randall J;
  • Hoogewerf, Arlene J;
  • Ackerman, Cheri M;
  • Armistead, Isaac O;
  • Baatenburg, Lara;
  • Borr, Matthew J;
  • Brouwer, Lindsay K;
  • Burkhart, Brandon J;
  • Bushhouse, Kelsey T;
  • Cesko, Lejla;
  • Choi, Tiffany YY;
  • Cohen, Heather;
  • Damsteegt, Amanda M;
  • Darusz, Jess M;
  • Dauphin, Cory M;
  • Davis, Yelena P;
  • Diekema, Emily J;
  • Drewry, Melissa;
  • Eisen, Michelle EM;
  • Faber, Hayley M;
  • Faber, Katherine J;
  • Feenstra, Elizabeth;
  • Felzer-Kim, Isabella T;
  • Hammond, Brandy L;
  • Hendriksma, Jesse;
  • Herrold, Milton R;
  • Hilbrands, Julia A;
  • Howell, Emily J;
  • Jelgerhuis, Sarah A;
  • Jelsema, Timothy R;
  • Johnson, Benjamin K;
  • Jones, Kelly K;
  • Kim, Anna;
  • Kooienga, Ross D;
  • Menyes, Erika E;
  • Nollet, Eric A;
  • Plescher, Brittany E;
  • Rios, Lindsay;
  • Rose, Jenny L;
  • Schepers, Allison J;
  • Scott, Geoff;
  • Smith, Joshua R;
  • Sterling, Allison M;
  • Tenney, Jenna C;
  • Uitvlugt, Chris;
  • VanDyken, Rachel E;
  • VanderVennen, Marielle;
  • Vue, Samantha;
  • Kokan, Nighat P;
  • Agbley, Kwabea;
  • Boham, Sampson K;
  • Broomfield, Daniel;
  • Chapman, Kayla;
  • Dobbe, Ali;
  • Dobbe, Ian;
  • Harrington, William;
  • Ibrahem, Marwan;
  • Kennedy, Andre;
  • Koplinsky, Chad A;
  • Kubricky, Cassandra;
  • Ladzekpo, Danielle;
  • Pattison, Claire;
  • Ramirez, Roman E;
  • Wande, Lucia;
  • Woehlke, Sarah;
  • Wawersik, Matthew;
  • Kiernan, Elizabeth;
  • Thompson, Jeffrey S;
  • Banker, Roxanne;
  • Bartling, Justina R;
  • Bhatiya, Chinmoy I;
  • Boudoures, Anna L;
  • Christiansen, Lena;
  • Fosselman, Daniel S;
  • French, Kristin M;
  • Gill, Ishwar S;
  • Havill, Jessen T;
  • Johnson, Jaelyn L;
  • Keny, Lauren J;
  • Kerber, John M;
  • Klett, Bethany M;
  • Kufel, Christina N;
  • May, Francis J;
  • Mecoli, Jonathan P;
  • Merry, Callie R;
  • Meyer, Lauren R;
  • Miller, Emily G;
  • Mullen, Gregory J;
  • Palozola, Katherine C;
  • Pfeil, Jacob J;
  • Thomas, Jessica G;
  • Verbofsky, Evan M;
  • Spana, Eric P;
  • Agarwalla, Anant;
  • Chapman, Julia;
  • Chlebina, Ben;
  • Chong, Insun;
  • Falk, IN;
  • Fitzgibbons, John D;
  • Friedman, Harrison;
  • Ighile, Osagie;
  • Kim, Andrew J;
  • Knouse, Kristin A;
  • Kung, Faith;
  • Mammo, Danny;
  • Ng, Chun Leung;
  • Nikam, Vinayak S;
  • Norton, Diana;
  • Pham, Philip;
  • Polk, Jessica W;
  • Prasad, Shreya;
  • Rankin, Helen;
  • Ratliff, Camille D;
  • Scala, Victoria;
  • Schwartz, Nicholas U;
  • Shuen, Jessica A;
  • Xu, Amy;
  • Xu, Thomas Q;
  • Zhang, Yi;
  • Rosenwald, Anne G;
  • Burg, Martin G;
  • Adams, Stephanie J;
  • Baker, Morgan;
  • Botsford, Bobbi;
  • Brinkley, Briana;
  • Brown, Carter;
  • Emiah, Shadie;
  • Enoch, Erica;
  • Gier, Chad;
  • Greenwell, Alyson;
  • Hoogenboom, Lindsay;
  • Matthews, Jordan E;
  • McDonald, Mitchell;
  • Mercer, Amanda;
  • Monsma, Nicholaus;
  • Ostby, Kristine;
  • Ramic, Alen;
  • Shallman, Devon;
  • Simon, Matthew;
  • Spencer, Eric;
  • Tomkins, Trisha;
  • Wendland, Pete;
  • Wylie, Anna;
  • Wolyniak, Michael J;
  • Robertson, Gregory M;
  • Smith, Samuel I;
  • DiAngelo, Justin R;
  • Sassu, Eric D;
  • Bhalla, Satish C;
  • Sharif, Karim A;
  • Choeying, Tenzin;
  • Macias, Jason S;
  • Sanusi, Fareed;
  • Torchon, Karvyn;
  • Bednarski, April E;
  • Alvarez, Consuelo J;
  • Davis, Kristen C;
  • Dunham, Carrie A;
  • Grantham, Alaina J;
  • Hare, Amber N;
  • Schottler, Jennifer;
  • Scott, Zackary W;
  • Kuleck, Gary A;
  • Yu, Nicole S;
  • Kaehler, Marian M;
  • Jipp, Jacob;
  • Overvoorde, Paul J;
  • Shoop, Elizabeth;
  • Cyrankowski, Olivia;
  • Hoover, Betsy;
  • Kusner, Matt;
  • Lin, Devry;
  • Martinov, Tijana;
  • Misch, Jonathan;
  • Salzman, Garrett;
  • Schiedermayer, Holly;
  • Snavely, Michael;
  • Zarrasola, Stephanie;
  • Parrish, Susan;
  • Baker, Atlee;
  • Beckett, Alissa;
  • Belella, Carissa;
  • Bryant, Julie;
  • Conrad, Turner;
  • Fearnow, Adam;
  • Gomez, Carolina;
  • Herbstsomer, Robert A;
  • Hirsch, Sarah;
  • Johnson, Christen;
  • Jones, Melissa;
  • Kabaso, Rita;
  • Lemmon, Eric;
  • Vieira, Carolina Marques Dos Santos;
  • McFarland, Darryl;
  • McLaughlin, Christopher;
  • Morgan, Abbie;
  • Musokotwane, Sepo;
  • Neutzling, William;
  • Nietmann, Jana;
  • Paluskievicz, Christina;
  • Penn, Jessica;
  • Peoples, Emily;
  • Pozmanter, Caitlin;
  • Reed, Emily;
  • Rigby, Nichole;
  • Schmidt, Lasse;
  • Shelton, Micah;
  • Shuford, Rebecca;
  • Tirasawasdichai, Tiara;
  • Undem, Blair;
  • Urick, Damian;
  • Vondy, Kayla;
  • Yarrington, Bryan;
  • Eckdahl, Todd T;
  • Poet, Jeffrey L;
  • Allen, Alica B;
  • Anderson, John E;
  • Barnett, Jason M;
  • Baumgardner, Jordan S;
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  • Mazur, Tammy;
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  • Melton, Amy D;
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  • Sandusky, Michael W;
  • Schmuecker, Samantha M;
  • Shipman, Anna L;
  • Smith, Anna L;
  • Thomsen, Kristen M;
  • Unzicker, Matthew R;
  • Vernon, William B;
  • Winn, Wesley W;
  • Woyski, Dustin S;
  • Zhu, Xiao;
  • Du, Chunguang;
  • Ament, Caitlin;
  • Aso, Soham;
  • Bisogno, Laura Simone;
  • Caronna, Jason;
  • Fefelova, Nadezhda;
  • Lopez, Lenin;
  • Malkowitz, Lorraine;
  • Marra, Jonathan;
  • Menillo, Daniella;
  • Obiorah, Ifeanyi;
  • Onsarigo, Eric Nyabeta;
  • Primus, Shekerah;
  • Soos, Mahdi;
  • Tare, Archana;
  • Zidan, Ameer;
  • Jones, Christopher J;
  • Aronhalt, Todd;
  • Bellush, James M;
  • Burke, Christa;
  • DeFazio, Steve;
  • Does, Benjamin R;
  • Johnson, Todd D;
  • Keysock, Nicholas;
  • Knudsen, Nelson H;
  • Messler, James;
  • Myirski, Kevin;
  • Rekai, Jade Lea;
  • Rempe, Ryan Michael;
  • Salgado, Michael S;
  • Stagaard, Erica;
  • Starcher, Justin R;
  • Waggoner, Andrew W;
  • Yemelyanova, Anastasia K;
  • Hark, Amy T;
  • Bertolet, Anne;
  • Kuschner, Cyrus E;
  • Parry, Kesley;
  • Quach, Michael;
  • Shantzer, Lindsey;
  • Shaw, Mary E;
  • Smith, Mary A;
  • Glenn, Omolara;
  • Mason, Portia;
  • Williams, Charlotte;
  • Key, S Catherine Silver;
  • Henry, Tyneshia CP;
  • Johnson, Ashlee G;
  • White, Jackie X;
  • Haberman, Adam;
  • Asinof, Sam;
  • Drumm, Kelly;
  • Freeburg, Trip;
  • Safa, Nadia;
  • Schultz, Darrin;
  • Shevin, Yakov;
  • Svoronos, Petros;
  • Vuong, Tam;
  • Wellinghoff, Jules;
  • Hoopes, Laura LM;
  • Chau, Kim M;
  • Ward, Alyssa;
  • Regisford, E Gloria C;
  • Augustine, LaJerald;
  • Davis-Reyes, Brionna;
  • Echendu, Vivienne;
  • Hales, Jasmine;
  • Ibarra, Sharon;
  • Johnson, Lauriaun;
  • Ovu, Steven;
  • Braverman, John M;
  • Bahr, Thomas J;
  • Caesar, Nicole M;
  • Campana, Christopher;
  • Cassidy, Daniel W;
  • Cognetti, Peter A;
  • English, Johnathan D;
  • Fadus, Matthew C;
  • Fick, Cameron N;
  • Freda, Philip J;
  • Hennessy, Bryan M;
  • Hockenberger, Kelsey;
  • Jones, Jennifer K;
  • King, Jessica E;
  • Knob, Christopher R;
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  • Perella, Mallory;
  • Ramsey, Kimberley;
  • Ramthun, Jennifer R;
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  • Robinett, Deirdre;
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  • Schueler, Mary Grace;
  • Shoemaker, Emma;
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  • Maffa, Amanda;
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  • Winters, Jenifer;
  • Yang, Bib;
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  • Ashrawi, Yara;
  • Benitez, Pedro;
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  • Bourland, Megan;
  • Chavez, Miranda;
  • Cruz, Samantha;
  • Elliott, GiNell;
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  • Flohr, Sarah;
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  • Fusco, Zach;
  • Goodwin, Zane;
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  • Raimey, England;
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  • Archambault, Alexi;
  • Chamma, Norma;
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  • Hammett, Deborah;
  • Kandahari, Adrese;
  • Khayrullina, Guzal;
  • Kumar, Sonali;
  • Lawrence, Samantha;
  • Madden, Nigel;
  • Mandelbaum, Max;
  • Milnthorp, Heather;
  • Mohini, Shiv;
  • Patel, Roshni;
  • Peacock, Sarah J;
  • Perling, Emily;
  • Quintana, Amber;
  • Rahimi, Michael;
  • Ramirez, Kristen;
  • Singhal, Rishi;
  • Weeks, Corinne;
  • Wong, Tiffany;
  • Gillis, Aubree T;
  • Moore, Zachary D;
  • Savell, Christopher D;
  • Watson, Reece;
  • Mel, Stephanie F;
  • Anilkumar, Arjun A;
  • Bilinski, Paul;
  • Castillo, Rostislav;
  • Closser, Michael;
  • Cruz, Nathalia M;
  • Dai, Tiffany;
  • Garbagnati, Giancarlo F;
  • Horton, Lanor S;
  • Kim, Dongyeon;
  • Lau, Joyce H;
  • Liu, James Z;
  • Mach, Sandy D;
  • Phan, Thu A;
  • Ren, Yi;
  • Stapleton, Kenneth E;
  • Strelitz, Jean M;
  • Sunjed, Ray;
  • Stamm, Joyce;
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  • Coomes, Daniel;
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  • Durchholz, Elaine J;
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  • Gross, Meleah J;
  • Gygi, Amber M;
  • Jackson, Lesley E;
  • Johnson, Amy;
  • Kocsisova, Zuzana;
  • Manghelli, Joshua L;
  • McNeil, Kylie;
  • Murillo, Michael;
  • Naylor, Kierstin L;
  • Neely, Jessica;
  • Ogawa, Emmy E;
  • Rich, Ashley;
  • Rogers, Anna;
  • Spencer, J Devin;
  • Stemler, Kristina M;
  • Throm, Allison A;
  • Van Camp, Matt;
  • Weihbrecht, Katie;
  • Wiles, T Aaron;
  • Williams, Mallory A;
  • Williams, Matthew;
  • Zoll, Kyle;
  • Bailey, Cheryl;
  • Zhou, Leming;
  • Balthaser, Darla M;
  • Bashiri, Azita;
  • Bower, Mindy E;
  • Florian, Kayla A;
  • Ghavam, Nazanin;
  • Greiner-Sosanko, Elizabeth S;
  • Karim, Helmet;
  • Mullen, Victor W;
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  • Zhang, Jiayu;
  • Rubin, Michael R;
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  • Colon-Vazquez, Mariela;
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Abstract

The Muller F element (4.2 Mb, ~80 protein-coding genes) is an unusual autosome of Drosophila melanogaster; it is mostly heterochromatic with a low recombination rate. To investigate how these properties impact the evolution of repeats and genes, we manually improved the sequence and annotated the genes on the D. erecta, D. mojavensis, and D. grimshawi F elements and euchromatic domains from the Muller D element. We find that F elements have greater transposon density (25-50%) than euchromatic reference regions (3-11%). Among the F elements, D. grimshawi has the lowest transposon density (particularly DINE-1: 2% vs. 11-27%). F element genes have larger coding spans, more coding exons, larger introns, and lower codon bias. Comparison of the Effective Number of Codons with the Codon Adaptation Index shows that, in contrast to the other species, codon bias in D. grimshawi F element genes can be attributed primarily to selection instead of mutational biases, suggesting that density and types of transposons affect the degree of local heterochromatin formation. F element genes have lower estimated DNA melting temperatures than D element genes, potentially facilitating transcription through heterochromatin. Most F element genes (~90%) have remained on that element, but the F element has smaller syntenic blocks than genome averages (3.4-3.6 vs. 8.4-8.8 genes per block), indicating greater rates of inversion despite lower rates of recombination. Overall, the F element has maintained characteristics that are distinct from other autosomes in the Drosophila lineage, illuminating the constraints imposed by a heterochromatic milieu.

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