Asexuality Associated with Marked Genomic Expansion of Tandemly Repeated rRNA and Histone Genes

Author:

McElroy Kyle E12ORCID,Müller Stefan3,Lamatsch Dunja K4,Bankers Laura5,Fields Peter D6ORCID,Jalinsky Joseph R2,Sharbrough Joel78,Boore Jeffrey L9,Logsdon John M2,Neiman Maurine210

Affiliation:

1. Ecology, Evolutionary, and Organismal Biology, Iowa State University, Ames, IA, USA

2. Department of Biology, University of Iowa, Iowa City, IA, USA

3. Institute of Human Genetics, Munich University Hospital, Ludwig-Maximilians University, Munich, Germany

4. Research Department for Limnology, University of Innsbruck, Mondsee, Mondsee, Austria

5. Division of Infectious Diseases, University of Colorado—Anschutz Medical Campus, Aurora, CO, USA

6. Department of Environmental Sciences, Zoology, University of Basel, Basel, Switzerland

7. Biology Department, New Mexico Institute of Mining and Technology, Socorro, NM, USA

8. Department of Biology, Colorado State University, Fort Collins, CO, USA

9. Providence St. Joseph Health and Institute for Systems Biology, Seattle, WA, USA

10. Department of Gender, Women's, and Sexuality Studies, University of Iowa, Iowa City, IA, USA

Abstract

Abstract How does asexual reproduction influence genome evolution? Although is it clear that genomic structural variation is common and important in natural populations, we know very little about how one of the most fundamental of eukaryotic traits—mode of genomic inheritance—influences genome structure. We address this question with the New Zealand freshwater snail Potamopyrgus antipodarum, which features multiple separately derived obligately asexual lineages that coexist and compete with otherwise similar sexual lineages. We used whole-genome sequencing reads from a diverse set of sexual and asexual individuals to analyze genomic abundance of a critically important gene family, rDNA (the genes encoding rRNAs), that is notable for dynamic and variable copy number. Our genomic survey of rDNA in P. antipodarum revealed two striking results. First, the core histone and 5S rRNA genes occur between tandem copies of the 18S–5.8S–28S gene cluster, a unique architecture for these crucial gene families. Second, asexual P. antipodarum harbor dramatically more rDNA–histone copies than sexuals, which we validated through molecular and cytogenetic analysis. The repeated expansion of this genomic region in asexual P. antipodarum lineages following distinct transitions to asexuality represents a dramatic genome structural change associated with asexual reproduction—with potential functional consequences related to the loss of sexual reproduction.

Funder

National Science Foundation

T. Anne Cleary International Dissertation Research Fellowship

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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