Disentangling the Causes for Faster-X Evolution in Aphids

Julie Jaquiéry; Jean Peccoud; Tiphaine Ouisse; Fabrice Legeai; Nathalie Prunier-Leterme; Anaïs Gouin; Pierre Nouhaud; Jennifer Brisson; Ryan Bickel; Swapna Purandare; Julie Poulain; Christophe Battail; Claire Lemaitre; Lucie Mieuzet; Gaël Le Trionnaire; Jean-Christophe Simon; Claude Rispe

Disentangling the Causes for Faster-X Evolution in Aphids

Julie Jaquiéry ^{1, 2} Jean Peccoud ^{3, 4} Tiphaine Ouisse ¹ Fabrice Legeai ^{2, 5} Nathalie Prunier-Leterme ² Anaïs Gouin ² Pierre Nouhaud ⁶ Jennifer Brisson ⁷ Ryan Bickel ⁷ Swapna Purandare ⁸ Julie Poulain ⁹ Christophe Battail ¹⁰ Claire Lemaitre ⁵ Lucie Mieuzet ² Gaël Le Trionnaire ² Jean-Christophe Simon ² Claude Rispe ¹¹

1 ECOBIO - Ecosystèmes, biodiversité, évolution [Rennes]

2 IGEPP - Institut de Génétique, Environnement et Protection des Plantes

3 EBI - Ecologie et biologie des interactions

4 EES - Ecologie, Evolution, Symbiose

5 GenScale - Scalable, Optimized and Parallel Algorithms for Genomics

Inria Rennes – Bretagne Atlantique , IRISA_D7 - GESTION DES DONNÉES ET DE LA CONNAISSANCE

6 Vetmeduni - University of Veterinary Medicine [Vienna]

7 University of Rochester [USA]

8 MCARS - Multidisciplinary Center for Advance Research and Studies

9 IG - Institut de Génomique d'Evry

10 CNG - Centre National de Génotypage

11 BIOEPAR - Biologie, Epidémiologie et analyse de risque en Santé Animale

Abstract : 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.

Keywords : sex-biased expression sex chromosome drift evolutionary rates selection hemizygosity

Document type :

Journal articles

Domain :

Life Sciences [q-bio]

Life Sciences [q-bio] / Ecology, environment

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