Suppressed recombination allows divergence between homologous sex chromosomes and the functionality of their genes. Here, we reveal patterns of the earliest stages of sex-chromosome evolution in the diploid dioecious herb Mercurialis annua on the basis of cytological analysis, de novo genome assembly and annotation, genetic mapping, exome resequencing of natural populations, and transcriptome analysis. The genome assembly contained 34,105 expressed genes, of which 10,076 were assigned to linkage groups. Genetic mapping and exome resequencing of individuals across the species range both identified the largest linkage group, LG1, as the sex chromosome. Although the sex chromosomes of M. annua are karyotypically homomorphic, we estimate that about one-third of the Y chromosome, containing 568 transcripts and spanning 22.3 cM in the corresponding female map, has ceased recombining. Nevertheless, we found limited evidence for Y-chromosome degeneration in terms of gene loss and pseudogenization, and most X- and Y-linked genes appear to have diverged in the period subsequent to speciation between M. annua and its sister species M. huetii, which shares the same sex-determining region. Taken together, our results suggest that the M. annua Y chromosome has at least two evolutionary strata: a small old stratum shared with M. huetii, and a more recent larger stratum that is probably unique to M. annua and that stopped recombining ∼1 MYA. Patterns of gene expression within the nonrecombining region are consistent with the idea that sexually antagonistic selection may have played a role in favoring suppressed recombination.

BIOGECO INRA University of Bordeaux 33610 Cestas France

Department of Biology Indiana University Bloomington IN 47405 Department of Ecology and Evolution University of Lausanne CH 1015 Switzerland

Department of Ecology and Evolution University of Lausanne CH 1015 Switzerland

Department of Ecology and Evolution University of Lausanne CH 1015 Switzerland Department of Integrative Biology University of Texas Austin 78712 Texas

Department of Ecology and Evolution University of Lausanne CH 1015 Switzerland Department of Plant Sciences University of Oxford OX1 3RB United Kingdom Department of Oncology John Radcliffe Hospital Oxford OX3 9DU United Kingdom

Department of Plant Developmental Genetics Institute of Biophysics Academy of Sciences of the Czech Republic 61200 Brno Czech Republic

Department of Plant Sciences University of Oxford OX1 3RB United Kingdom

Laboratoire Biométrie et Biologie Évolutive CNRS Université Lyon 1 69100 Villeurbanne France

University of Helsinki Institute of Biotechnology 00014 Finland

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