Y chromosomes have come and gone many times during evolutionary history. Take beetles. When Heath Blackmon and Jeff Demuth modeled sex chromosome evolution in more than a thousand beetle species, they found the Y chromosome had independently evolved around 65 times in the suborder Adephaga alone. And as fast as this group evolved new Y chromosomes, it lost them at roughly the same pace.

But when it came to the other main suborder of beetles, the Polyphaga, Y chromosomes turned out to be unexpectedly stable. In this group, Ys seemed to be lost only about half as fast as they were gained.

So what’s the difference? Why are Y chromosomes lost at a much slower rate in Polyphaga?

In the June issue of GENETICS, Blackmon and Demuth, in the new GSA Journals “Genetics of Sex” collection, describe their intriguing findings and propose an explanation—the “fragile Y” hypothesis— that points the finger at the mechanics of meiosis.

The authors used the enormous diversity of beetles to gain a bird’s-eye view of sex chromosome evolution. Beetles are a rich source of phylogenetic data because there are so many species—more than in any other eukaryotic order. By combing the literature for published beetle karyotypes, the authors catalogued over 4000 species and classified them into three groups according to their sex chromosome system: XY, XO, or XY with distance pairing.

In XY systems, females carry two Xs and males carry an X and a Y. In XO species, the Y chromosome has been lost from the lineage and males carry only one X chromosome. The third category covers species that use an XY system but have evolved an unconventional mechanism for pairing the X and Y at meiosis. In distance pairing, rather than the familiar synaptic line-up of X and Y that allows crossing-over before segregation, the X and Y pair while at a distance from each other and do not recombine.

Using these data in combination with a phylogeny of 1,126 of taxa, the team estimated rates of Y chromosome gain and loss. Besides finding the curiously slow rate of loss in Polyphaga compared to Adephaga, they noted another striking difference between the suborders: none of the Adephaga species in the study used an XY distance pairing system, while 60 percent of Polyphaga species did. This pattern inspired the authors to develop the fragile Y hypothesis.

It is well known that Y chromosomes (and the female heterogametic equivalents, W chromosomes) are prone to decay, losing genes over time. This deterioration is thought to be partly caused by selection to suppress recombination between the X and Y. Reduced recombination helps maintain linkage between the sex-determining region and alleles that are beneficial in one sex but detrimental in the other.

In Blackmon and Demuth’s hypothesis, as the recombining (“pseudoautosomal”) portion of the Y shrinks, the opportunities for chiasmata formation also decrease. Because proper segregation normally depends on these crossover sites, the probability of losing the Y chromosome at meiosis should therefore increase.

But as we’ve seen, not all species depend on chiasmata for segregation of X and Y. The fragile Y hypothesis predicts that achiasmatic XY segregation mechanisms, such as distance pairing, should be favored as the pseudoautosomal region gets smaller. Therefore in lineages that evolve such mechanisms, the Y chromosome is much less likely to be missorted and lost. Consistent with this hypothesis, lower rates of Y chromosome loss were found among Adephaga clades that use achiasmatic pairing.

The significance of the hypothesis reaches far beyond beetles. Among mammals, the eutherian species with the smallest pseudoautosomal regions seem to have repeatedly evolved either achiasmatic meiosis or Y chromosome loss, exactly as the fragile Y hypothesis predicts.

This study, the largest of its kind, shows that the dizzying abundance of beetle species can provide important insights into sex chromosome evolution. Higher resolution genomic approaches will have even greater power to reveal the fine details of the comings and goings of sex chromosomes and the many evolutionary forces that drive them.

 

Blackmon H. and J.P. Demuth (2014). Estimating Tempo and Mode of Y Chromosome Turnover: Explaining Y Chromosome Loss With the Fragile Y Hypothesis, GENETICS, 197 (2) 561-572. DOI: http://dx.doi.org/10.1534/genetics.114.164269

, , ,

Cristy Gelling is a science writer, lapsed yeast geneticist, and former Communications Director at the GSA.

View all posts by Cristy Gelling »

Read more in

  • Early Career Leadership Spotlight: Julio Molina Pineda 

    We’re taking time to get to know the members of the GSA’s Early Career Scientist Committees. Join us to learn more about our early career scientist advocates. Julio Molina Pineda  Policy and Advocacy University of Arkansas Research Interest  My research interests focus on using model organisms to genetically dissect complex traits related to human disease. My…

  • Peiwei Chen

    Early Career Leadership Spotlight: Peiwei Chen

    We’re taking time to get to know the members of the GSA’s Early Career Scientist Committees. Join us to learn more about our early career scientist advocates. Peiwei Chen Accessibility Subcommittee California Institute of Technology Research Interest Far from a harmonious place, the genome is a battleground, where every bit of DNA fights for inheritance and…

  • #Dros23 GSA Poster Award winners

    We are pleased to announce the GSA Poster Award winners from the 64th Annual Drosophila Research Conference! Undergraduate and graduate student members of the GSA were eligible for the awards, and a hard-working team of postdocs volunteered their time as judges. Congratulations to all! Undergraduate Students 1st Place: Sofia Karter Lopez, University of Toronto “Rab11 mediates E-cadherin recycling during…

  • Congratulations to the Fall 2022 DeLill Nasser Awardees!

    GSA is pleased to announce the recipients of the DeLill Nasser Award for Professional Development in Genetics for Fall 2022! Given twice a year to graduate students and postdoctoral researchers, DeLill Nasser Awards support attendance at meetings and laboratory courses. The award is named in honor of DeLill Nasser, a long-time GSA supporter and National Science Foundation…

  • GENETICS & G3 editors

    New editors join GENETICS, G3 editorial boards

    Several new editors are joining the GSA Journals. We’re excited to welcome Ricardo Zayas to the GENETICS editorial board under the Molecular Genetics of Development section, and on the G3: Genes|Genomes|Genetics board, we welcome Polly Campbell, Kevin Vogel, Joe Parker, and Ricardo Mallarino. Ricardo Zayas Associate Editor Ricardo Zayas is a Professor of Biology at…

  • Worms and Flies Provide Key Clues to Medical Mystery

    This article is part of a series of posts outlining the history and impact of research in experimental organisms. The series is developed in collaboration with the GSA Public Communications and Engagement Committee. By the time Bertrand Might was six months old, it was clear something was amiss. His muscles weren’t developing normally; he was…

  • Congratulations to the 2023 Early Career Leadership Program Cohort!

    The Genetics Society of America (GSA) is excited to announce the latest cohort of student, postdoc, and early-career research leaders joining the Early Career Leadership Program.  Participants receive training and mentoring while serving on committees charged with understanding the needs, interests, concerns, and challenges of early career scientist members of the GSA. As part of…

  • 64th Annual Drosophila Research Conference March 1–5, 2023 Chicago, IL and online

    GSA LOCI: Local Outreach Community Initiatives @ GSA Conferences

    Highlights: Local Outreach Community Initiatives (LOCI): The Genetics Society of America is committed to supporting the communities of the host cities of our conferences. This new year, we are excited to reconnect with our GSA community in meaningful ways within and beyond our existing programming. The GSA membership has created a caring and supportive environment…

  • Headshots of the 5 elected members of the GSA Board of Directors on a black background.

    New members of the GSA Board of Directors: 2023–2025

    We are pleased to announce the election of five new leaders to the GSA Board of Directors: 2023 Vice President/2024 President Mariana Wolfner Distinguished Professor of Molecular Biology and Genetics and Stephen H. Weiss Presidential Fellow My research has focused on the genes and pathways that mediate sexual development and reproduction, primarily in Drosophila. From…

  • Lance David Miller

    Lance David Miller: Lighting Your Own Fire by Finding the Right Resources

    By Daniel J. Gironda In the Paths to Science Policy series, we talk to individuals who have a passion for science policy and are active in advocacy through their various roles and careers. The series aims to inform and guide early career scientists interested in science policy. This series is brought to you by the…

  • Graça Almeida-Porada: The Importance of Communication in a Technologically Advancing World

    By Daniel J. Gironda In the Paths to Science Policy series, we talk to individuals who have a passion for science policy and are active in advocacy through their various roles and careers. The series aims to inform and guide early career scientists interested in science policy. This series is brought to you by the…