“…Knowledge about the biology and evolution of sex chromosomes stems from a few well-studied model organisms, notably mammals, birds, fish and Drosophila 6 . While studies so far have primarily focused on diploid sex determination systems (the classical XX/XY or ZW/ZZ systems), haploid phase sex-determination systems (U/V systems) such as those of mosses and brown, red and green algae 7,8 remain largely unexplored.…”
Sex chromosomes fall into three classes: XX/XY, ZW/ZZ and U/V systems. The rise, evolution and demise of U/V systems have remained enigmatic to date. Here, we analyze genomes spanning the entire brown algal phylogeny to decipher their sex-determination evolutionary history. The birth of U/V sex chromosomes evolved more than 250 million years ago, when a pivotal male-determinant located in a discrete region in proto-U and proto-V chromosomes ceased recombining. Over time, nested inversions led to step-wise expansions, accompanying increasing morphological complexity and sexual differentiation of brown seaweeds. Unlike XX/XY and ZW/ZZ, U/V evolve mainly by gene gain, showing minimal degeneration. They are structurally dynamic, and act as genomic 'cradles' fostering the birth of new genes. Our analyses show that hermaphroditism arose from ancestral males that acquired U-specific genes by ectopic recombination, and that in the transition from a U/V to an XX/XY system, V-specific genes moved down the genetic hierarchy of sex determination. Both events lead to the demise of U and V and erosion of their specific genomic characteristics. Taken together, our findings offer a comprehensive model of U/V sex chromosome evolution.
“…Knowledge about the biology and evolution of sex chromosomes stems from a few well-studied model organisms, notably mammals, birds, fish and Drosophila 6 . While studies so far have primarily focused on diploid sex determination systems (the classical XX/XY or ZW/ZZ systems), haploid phase sex-determination systems (U/V systems) such as those of mosses and brown, red and green algae 7,8 remain largely unexplored.…”
Sex chromosomes fall into three classes: XX/XY, ZW/ZZ and U/V systems. The rise, evolution and demise of U/V systems have remained enigmatic to date. Here, we analyze genomes spanning the entire brown algal phylogeny to decipher their sex-determination evolutionary history. The birth of U/V sex chromosomes evolved more than 250 million years ago, when a pivotal male-determinant located in a discrete region in proto-U and proto-V chromosomes ceased recombining. Over time, nested inversions led to step-wise expansions, accompanying increasing morphological complexity and sexual differentiation of brown seaweeds. Unlike XX/XY and ZW/ZZ, U/V evolve mainly by gene gain, showing minimal degeneration. They are structurally dynamic, and act as genomic 'cradles' fostering the birth of new genes. Our analyses show that hermaphroditism arose from ancestral males that acquired U-specific genes by ectopic recombination, and that in the transition from a U/V to an XX/XY system, V-specific genes moved down the genetic hierarchy of sex determination. Both events lead to the demise of U and V and erosion of their specific genomic characteristics. Taken together, our findings offer a comprehensive model of U/V sex chromosome evolution.
“…Sex chromosome-autosome (Sex-A) fusions contribute to the evolution of neo-sex chromosomes (1,2), but it remains unclear what promotes them. Sexually antagonistic selection, direct selection, genetic drift, meiotic drive, and sheltering of deleterious mutations have all been suggested as possible drivers of Sex-A fusions (3)(4)(5)(6).…”
Sex chromosomes are evolutionarily labile in many animals, and fusion with an autosome is one of the mechanisms by which they can evolve. Sex chromosome-autosome (SA) fusions can reduce sexual conflict and promote adaptation and reproductive isolation among species. Recently, advances in genomics have fuelled the discovery of SA fusions in multiple vertebrates and in some invertebrates such as Lepidoptera. Here, we discovered multiple SA fusions in the sara/sapho clade of the classical adaptive radiation of Heliconius butterflies. While the vast majority of Heliconius species have 21 chromosomes, species of this particularly rapidly diversifying clade have up to 60 chromosomes. We found a sex chromosome fusion with chromosome 4 at the base of the sapho clade and two additional sex chromosome fusions, each shared by two species. These sequential fusions between autosomes and sex chromosomes make the Heliconius sapho clade an ideal system to study the role of neo-sex chromosomes in adaptive radiations and the degeneration of sex chromosomes over time. Our study adds to a growing number of examples in butterflies that, in the future, may help to unravel the importance of such rearrangements in the evolution of Lepidoptera and animals in general.
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