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Studies of sex chromosomes have played a central role in understanding the consequences of suppressed recombination and sex-specific inheritance among several genomic phenomena. However, we argue that these efforts will benefit from a more rigorous examination of haploid UV sex chromosome systems, in which both the female-limited (U) and male-limited (V) experience suppressed recombination and sex-limited inheritance, and both are transcriptionally active in the haploid and diploid states. We review the life cycle differences that generate UV sex chromosomes and genomic data showing that ancient UV systems have evolved independently in many eukaryotic groups, but gene movement on and off the sex chromosomes, and potentially degeneration continue to shape the current gene content of the U and V chromosomes. Although both theory and empirical data show that the evolution of UV sex chromosomes is shaped by many of the same processes that govern diploid sex chromosome systems, we highlight how the symmetrical inheritance between the UV chromosomes provide an important test of sex-limited inheritance in shaping genome architecture. We conclude by examining how genetic conflict (over sexual dimorphism, transmission-ratio distortion, or parent-offspring conflict) may drive gene gain on UV sex chromosomes, and highlight the role of breeding system in governing the action of these processes. Collectively these observations demonstrate the potential for evolutionary genomic analyses of varied UV sex chromosome systems, combined with natural history studies, to understand how genetic conflict shapes sex chromosome gene content.

Centro de Investigación Forestal (CIFOR), Nonrecombining sex chromosomes, like the mammalian Y, often lose genes and accumulate transposable ele ments, a process termed degeneration. The correlation between suppressed recombination and degeneration is clear in animal XY systems, but the absence of recombination is confounded with other asymmetries between the X and Y. In contrast, UV sex chromosomes, like those found in bryophytes, experience symmetrical population genetic conditions. Here, we generate nearly gapless female and male chromosome-scale reference genomes of the moss Ceratodon purpureus to test for degeneration in the bryophyte UV sex chromosomes. We show that the moss sex chromosomes evolved over 300 million years ago and expanded via two chromosomal fusions. Although the sex chromosomes exhibit weaker purifying selection than autosomes, we find that suppressed recombination alone is insufficient to drive degeneration. Instead, the U and V sex chromosomes harbor thousands of broadly expressed genes, including numerous key regulators of sexual development across land plants., This work was supported by NSF DEB-1541005 and 1542609 and start-up funds from UF to S.F.M.; microMORPH Cross-Disciplinary Training Grant, Sigma-Xi Grant-In-Aid of Research, and Society for the Study of Evolution Rosemary Grant Award to S.B.C.; NSF DEB-1239992 to N.J.W.; the Emil Aaltonen Foundation and the University of Turku to S.O.; and NSF DEB-1541506 to J.G.B. and S.F.M. The work conducted by the U.S. Department of Energy Joint Genome Institute was supported by the Office of Science of the U.S. Department of Energy under contract no. DE-AC02-05CH11231., 12 Pág. Supplementary material for this article is available at http://advances.sciencemag.org/cgi/ content/full/7/27/eabh2488/DC1

A central problem in evolutionary biology is to identify the forces that maintain genetic variation for fitness in natural populations. Sexual antagonism, in which selection favours different variants in males and females, can slow the transit of a polymorphism through a population or can actively maintain fitness variation. The amount of sexually antagonistic variation to be expected depends in part on the genetic architecture of sexual dimorphism, about which we know relatively little. Here, we used a multivariate quantitative genetic approach to examine the genetic architecture of sexual dimorphism in a scent-based fertilization syndrome of the moss Ceratodon purpureus. We found sexual dimorphism in numerous traits, consistent with a history of sexually antagonistic selection. The cross-sex genetic correlations (r(mf)) were generally heterogeneous with many values indistinguishable from zero, which typically suggests that genetic constraints do not limit the response to sexually antagonistic selection. However, we detected no differentiation between the female- and male-specific trait (co)variance matrices (G(f) and G(m), respectively), meaning the evolution of sexual dimorphism may be constrained. The cross-sex cross-trait covariance matrix B contained both symmetric and asymmetric elements, indicating that the response to sexually antagonistic or sexually concordant selection, and the constraint to sexual dimorphism, are highly dependent on the traits experiencing selection. The patterns of genetic variances and covariances among these fitness components is consistent with partly sex-specific genetic architectures having evolved in order to partially resolve multivariate genetic constraints (i.e. sexual conflict), enabling the sexes to evolve towards their sex-specific multivariate trait optima.

Non-recombining sex chromosomes, like the mammalian Y, often lose genes and accumulate transposable elements, a process termed degeneration1,2. The correlation between suppressed recombination and degeneration is clear in animal XY systems1,2, but the absence of recombination is confounded with other asymmetries between the X and Y. In contrast, UV sex chromosomes, like those found in bryophytes, experience symmetrical population genetic conditions3,4. Here we test for degeneration in the bryophyte UV sex chromosome system through genomic comparisons with new female and male chromosome-scale reference genomes of the moss Ceratodon purpureus. We show that the moss sex chromosomes evolved over 300 million years ago and expanded via two chromosomal fusions. Although the sex chromosomes show signs of weaker purifying selection than autosomes, we find suppressed recombination alone is insufficient to drive gene loss on sex-specific chromosomes. Instead, the U and V sex chromosomes harbor thousands of broadly-expressed genes, including numerous key regulators of sexual development across land plants.

A central problem in evolutionary biology is to identify the forces that maintain genetic variation for fitness in natural populations. Sexual antagonism, in which selection favours different variants in males and females, can slow the transit of a polymorphism through a population or can actively maintain fitness variation. The amount of sexually antagonistic variation to be expected depends in part on the genetic architecture of sexual dimorphism, about which we know relatively little. Here, we used a multivariate quantitative genetic approach to examine the genetic architecture of sexual dimorphism in a scent-based fertilization syndrome of the mossCeratodon purpureus.We found sexual dimorphism in numerous traits, consistent with a history of sexually antagonistic selection. The cross-sex genetic correlations (rmf) were generally heterogeneous with many values indistinguishable from zero, which typically suggests that genetic constraints do not limit the response to sexually antagonistic selection. However, we detected no differentiation between the female- and male-specific trait (co)variance matrices (GfandGm, respectively), meaning the evolution of sexual dimorphism may be constrained. The cross-sex cross-trait covariance matrixBcontained both symmetric and asymmetric elements, indicating that the response to sexually antagonistic or sexually concordant selection, and the constraint to sexual dimorphism, are highly dependent on the traits experiencing selection. The patterns of genetic variances and covariances among these fitness components is consistent with partly sex-specific genetic architectures having evolved in order to partially resolve multivariate genetic constraints (i.e. sexual conflict), enabling the sexes to evolve towards their sex-specific multivariate trait optima.