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The Evolutionary Tempo of Sex Chromosome Degradation in Carica papaya

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Abstract

Genes on non-recombining heterogametic sex chromosomes may degrade over time through the irreversible accumulation of deleterious mutations. In papaya, the non-recombining male-specific region of the Y (MSY) consists of two evolutionary strata corresponding to chromosomal inversions occurring approximately 7.0 and 1.9 MYA. The step-wise recombination suppression between the papaya X and Y allows for a temporal examination of the degeneration progress of the young Y chromosome. Comparative evolutionary analyses of 55 X/Y gene pairs showed that Y-linked genes have more unfavorable substitutions than X-linked genes. However, this asymmetric evolutionary pattern is confined to the oldest stratum, and is only observed when recently evolved pseudogenes are included in the analysis, indicating a slow degeneration tempo of the papaya Y chromosome. Population genetic analyses of coding sequence variation of six Y-linked focal loci in the oldest evolutionary stratum detected an excess of nonsynonymous polymorphism and reduced codon bias relative to autosomal loci. However, this pattern was also observed for corresponding X-linked loci. Both the MSY and its corresponding X-specific region are pericentromeric where recombination has been shown to be greatly reduced. Like the MSY region, overall selective efficacy on the X-specific region may be reduced due to the interference of selective forces between highly linked loci, or the Hill–Robertson effect, that is accentuated in regions of low or suppressed recombination. Thus, a pattern of gene decay on the X-specific region may be explained by relaxed purifying selection and widespread genetic hitchhiking due to its pericentromeric location.

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Acknowledgments

We thank two anonymous reviewers for their helpful comments in preparing this manuscript. This work was supported by the National Science Foundation (DBI-0922545) to RCM and by the Department of Botany at Miami University through Academic Challenge grants to MW. We are greatly indebted to Oscar Rocha at Kent State University for his help during the specimen collecting process in Costa Rica. We would also like to thank our collaborators Ray Ming (University of Illinois at Urbana-Champaign) and Qingyi Yu (Texas A&M University) for providing papaya sequence information and cultivar tissues.

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  1. Meng Wu

    Present address: Evolution, Ecology & Behavior Graduate Program, Department of Biology, Indiana University, Bloomington, IN, 47405, USA

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  1. Botany Graduate Program, Department of Biology, Miami University, Oxford, OH, 45056, USA

    Meng Wu & Richard C. Moore

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  1. Meng Wu
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Correspondence to Richard C. Moore.

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Wu, M., Moore, R.C. The Evolutionary Tempo of Sex Chromosome Degradation in Carica papaya . J Mol Evol 80, 265–277 (2015). https://doi.org/10.1007/s00239-015-9680-1

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