Until recently, the field of sex chromosome evolution has been dominated by the canonical unidirectional scenario, first developed by Muller in 1918. This model postulates that sex chromosomes emerge from autosomes by acquiring a sex-determining locus. Recombination reduction then expands outwards from this locus, to maintain its linkage with sexually antagonistic/advantageous alleles, resulting in Y or W degeneration and potentially culminating in their disappearance. Based mostly on empirical vertebrate research, we challenge and expand each conceptual step of this canonical model and present observations by numerous experts in two parts of a theme issue of Phil. Trans. R. Soc. B. We suggest that greater theoretical and empirical insights into the events at the origins of sex-determining genes (rewiring of the gonadal differentiation networks), and a better understanding of the evolutionary forces responsible for recombination suppression are required. Among others, crucial questions are: Why do sex chromosome differentiation rates and the evolution of gene dose regulatory mechanisms between male versus female heterogametic systems not follow earlier theory? Why do several lineages not have sex chromosomes? And: What are the consequences of the presence of (differentiated) sex chromosomes for individual fitness, evolvability, hybridization and diversification? We conclude that the classical scenario appears too reductionistic. Instead of being unidirectional, we show that sex chromosome evolution is more complex than previously anticipated and principally forms networks, interconnected to potentially endless outcomes with restarts, deletions and additions of new genomic material. This article is part of the theme issue 'Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)'.

Amphibian Research Center Hiroshima University Higashi Hiroshima 739 8526 Japan

Department of Ecology and Evolution University of Lausanne CH 1015 Lausanne Switzerland

Department of Ecology Evolution and Organismal Biology Iowa State University Ames IA 50011 USA

Department of Ecology Faculty of Science Charles University Viničná 7 Prague Czech Republic

Department of Experimental Biology Faculty of Experimental Sciences University of Jaén Las Lagunillas Campus S N 23071 Jaén Spain

INRAE LPGP 35000 Rennes France

Institute of Animal Physiology and Genetics Czech Academy of Sciences Rumburská 89 Liběchov Czech Republic

Institute of Ecology and Evolution University of Bern CH 3012 Bern Switzerland

Leibniz Institute of Freshwater Ecology and Inland Fisheries IGB Müggelseedamm 301 12587 Berlin Germany

State Key Laboratory of Developmental Biology of Freshwater Fish College of Life Sciences Hunan Normal University Changsha 410081 Hunan People's Republic of China

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Advances in Understanding the Karyotype Evolution of Tetrapulmonata and Two Other Arachnid Taxa, Ricinulei and Solifugae

Satellite DNAs and the evolution of the multiple X1X2Y sex chromosomes in the wolf fish Hoplias malabaricus (Teleostei; Characiformes)

Heteromorphic ZZ/ZW sex chromosomes sharing gene content with mammalian XX/XY are conserved in Madagascan chameleons of the genus Furcifer

Madagascar Leaf-Tail Geckos (Uroplatus spp.) Share Independently Evolved Differentiated ZZ/ZW Sex Chromosomes

ZZ/ZW Sex Chromosomes in the Madagascar Girdled Lizard, Zonosaurus madagascariensis (Squamata: Gerrhosauridae)

Cytogenetic Analysis of the Members of the Snake Genera Cylindrophis, Eryx, Python, and Tropidophis

Preface