Extensive Recombination Suppression and Epistatic Selection Causes Chromosome-Wide Differentiation of a Selfish Sex Chromosome in .

TitleExtensive Recombination Suppression and Epistatic Selection Causes Chromosome-Wide Differentiation of a Selfish Sex Chromosome in .
Publication TypeJournal Article
Year of Publication2020
AuthorsFuller, ZL, Koury, SA, Leonard, CJ, Young, RE, Ikegami, K, Westlake, J, Richards, S, Schaeffer, SW, Phadnis, N
Date Published2020 Sep
KeywordsAnimals, Chromosome Inversion, Drosophila, Epistasis, Genetic, Evolution, Molecular, Genes, Modifier, Linkage Disequilibrium, Recombination, Genetic, Selection, Genetic, Suppression, Genetic, X Chromosome

() chromosomes are selfish -chromosomes that distort Mendelian segregation and are commonly associated with inversions. These chromosomal rearrangements suppress recombination with Standard () -chromosomes and are hypothesized to maintain multiple alleles important for distortion in a single large haplotype. Here, we conduct a multifaceted study of the multiply inverted chromosome to understand the evolutionary history, genetic architecture, and present-day dynamics that shape this enigmatic selfish chromosome. The chromosome has three nonoverlapping inversions of the right arm of the metacentric -chromosome: basal, medial, and terminal. We find that 23 of 29 Mb of the -chromosome right arm is highly differentiated between the Standard and arrangements, including a 6.6 Mb collinear region between the medial and terminal inversions. Although crossing-over is heavily suppressed on this chromosome arm, we discover it is not completely eliminated, with measured rates indicating recombination suppression alone cannot explain patterns of differentiation or the near-perfect association of the three chromosome inversions in nature. We then demonstrate the ancient basal and medial inversions of the chromosome contain genes sufficient to cause weak distortion. In contrast, the younger terminal inversion cannot distort by itself, but contains at least one modifier gene necessary for full manifestation of strong sex chromosome distortion. By parameterizing population genetic models for chromosome-wide linkage disequilibrium with our experimental results, we infer that strong selection acts to maintain the near-perfect association of chromosome inversions in present-day populations. Based on comparative genomic analyses, direct recombination experiments, segregation distortion assays, and population genetic modeling, we conclude the combined action of suppressed recombination and strong, ongoing, epistatic selection shape the arrangement into a highly differentiated chromosome.

Alternate JournalGenetics
PubMed ID32732371
PubMed Central IDPMC7463281
Grant ListR01 GM098478 / GM / NIGMS NIH HHS / United States
T32 GM102057 / GM / NIGMS NIH HHS / United States
R01 GM115914 / GM / NIGMS NIH HHS / United States

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