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Genome Biol Evol. 2018 Feb 1;10(2):507-520. doi: 10.1093/gbe/evy015.

Disentangling the Causes for Faster-X Evolution in Aphids.

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INRA UMR IGEPP Domaine de la Motte, Le Rheu, France.
CNRS UMR 6553 ECOBIO, Université de Rennes 1, France.
CNRS UMR 7267 Ecologie et Biologie des Interactions, Equipe Ecologie Evolution Symbiose, Université de Poitiers, France.
INRIA Centre Rennes - Bretagne Atlantique, GenOuest, Rennes, France.
Institute of Population Genetics, Vetmeduni Vienna, Vienna, Austria.
Department of Biology, University of Rochester.
Multidisciplinary Center for Advance Research and Studies (MCARS), Jamia Millia Islamia, New Delhi, India.
Commissariat à l'Energie Atomique (CEA), Institut de Génomique (IG), Genoscope, Evry, France.
Commissariat à l'Energie Atomique (CEA), Institut de Génomique (IG), Centre National de Génotypage (CNG), Evry, France.
BIOEPAR, INRA, ONIRIS, La Chantrerie, Nantes, France.


The faster evolution of X chromosomes has been documented in several species, and results from the increased efficiency of selection on recessive alleles in hemizygous males and/or from increased drift due to the smaller effective population size of X chromosomes. Aphids are excellent models for evaluating the importance of selection in faster-X evolution because their peculiar life cycle and unusual inheritance of sex chromosomes should generally lead to equivalent effective population sizes for X and autosomes. Because we lack a high-density genetic map for the pea aphid, whose complete genome has been sequenced, we first assigned its entire genome to the X or autosomes based on ratios of sequencing depth in males (X0) to females (XX). Then, we computed nonsynonymous to synonymous substitutions ratios (dN/dS) for the pea aphid gene set and found faster evolution of X-linked genes. Our analyses of substitution rates, together with polymorphism and expression data, showed that relaxed selection is likely to be the greatest contributor to faster-X because a large fraction of X-linked genes are expressed at low rates and thus escape selection. Yet, a minor role for positive selection is also suggested by the difference between substitution rates for X and autosomes for male-biased genes (but not for asexual female-biased genes) and by lower Tajima's D for X-linked compared with autosomal genes with highly male-biased expression patterns. This study highlights the relevance of organisms displaying alternative chromosomal inheritance to the understanding of forces shaping genome evolution.


drift; evolutionary rates; hemizygosity; selection; sex chromosome; sex-biased expression

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