Judith E. Mank

Sex Determination: Why So Many Ways of Doing It?

Sex is universal amongst most eukaryotes, yet a remarkable diversity of sex determining mechanisms exists. We review our current understanding of how and why sex determination evolves in animals and plants.

Are all sex chromosomes created equal

Three principal types of chromosomal sex determination are found in nature: male heterogamety (XY systems, as in mammals), female heterogamety (ZW systems, as in birds), and haploid phase determination (UV systems, as in some algae and bryophytes). Although these systems share many common features, there are important biological differences between them that have broad evolutionary and genomic implications. Here we combine theoretical predictions with empirical observations to discuss how differences in selection, genetic properties and transmission uniquely shape each system. We elucidate how the differences among these systems can be exploited to gain insights about general evolutionary processes, genome structure, and gene expression. We suggest directions for research that will greatly increase our general understanding of the forces driving sex-chromosome evolution in diverse organisms.

Sex Chromosomes and the Evolution of Sexual Dimorphism: Lessons from the Genome

Females and males of many animals exhibit a striking array of sexual dimorphisms, ranging from the primary differences of the gametes and gonads to the somatic differences often seen in behavior, morphology, and physiology. These differences raise many questions regarding how such divergent phenotypes can arise from a genome that is largely shared between the sexes. Recent progress in genomics has revealed some of the actual genetic mechanisms that create separate sex‐specific phenotypes, and the evidence indicates that thousands of genes across all portions of the genome contribute to male and female forms through sex‐biased gene expression. Related work has begun to define the strength and influence of sex‐specific evolutionary forces that shape these phenotypic dimorphisms and how they in turn affect the genome. Additionally, theory has long suggested that the evolution of sexual dimorphism is facilitated by sex chromosomes, as these are the only portions of the genome that differ between males and females. Genomic analysis indicates that there is indeed a relationship between sexual dimorphism and the sex chromosomes. However, the connection is far more complicated than current theory allows, and this may ultimately require a reexamination of the assumptions so that predictions match the accumulating empirical data.

EFFECTIVE POPULATION SIZE AND THE FASTER-X EFFECT: EMPIRICAL RESULTS AND THEIR INTERPRETATION

The X or Z chromosome has several characteristics that distinguish it from the autosomes, namely hemizygosity in the heterogametic sex, and a potentially different effective population size, both of which may influence the rate and nature of evolution. In particular, there may be an accelerated rate of adaptive change for X‐linked compared to autosomal coding sequences, often referred to as the Faster‐X effect. Empirical studies have indicated that the strength of Faster‐X evolution varies among different species, and theoretical treatments have shown that demography and mating system can substantially affect the degree of Faster‐X evolution. Here we integrate genomic data on Faster‐X evolution from a variety of animals with the demographic factors, mating system, and sex chromosome regulatory characteristics that may influence it. Our results suggest that differences in effective population size and mechanisms of dosage compensation may influence the perceived extent of Faster‐X evolution, and help to explain several clade‐specific patterns that we observe.

The Birds and the Bees and the Flowers and the Trees: Lessons from Genetic Mapping of Sex Determination in Plants and Animals

The ability to identify genetic markers in nonmodel systems has allowed geneticists to construct linkage maps for a diversity of species, and the sex-determining locus is often among the first to be mapped. Sex determination is an important area of study in developmental and evolutionary biology, as well as ecology. Its importance for organisms might suggest that sex determination is highly conserved. However, genetic studies have shown that sex determination mechanisms, and the genes involved, are surprisingly labile. We review studies using genetic mapping and phylogenetic inferences, which can help reveal evolutionary pattern within this lability and potentially identify the changes that have occurred among different sex determination systems. We define some of the terminology, particularly where confusion arises in writing about such a diverse range of organisms, and highlight some major differences between plants and animals, and some important similarities. We stress the importance of studying taxa suitable for testing hypotheses, and the need for phylogenetic studies directed to taxa where the patterns of changes can be most reliably inferred, if the ultimate goal of testing hypotheses regarding the selective forces that have led to changes in such an essential trait is to become feasible.

PHYLOGENETIC PERSPECTIVES IN THE EVOLUTION OF PARENTAL CARE IN RAY-FINNED FISHES

Abstract Among major vertebrate groups, ray‐finned fishes (Actinopterygii) collectively display a nearly unrivaled diversity of parental care activities. This fact, coupled with a growing body of phylogenetic data for Actinopterygii, makes these fishes a logical model system for analyzing the evolutionary histories of alternative parental care modes and associated reproductive behaviors. From an extensive literature review, we constructed a supertree for ray‐finned fishes and used its phylogenetic topology to investigate the evolution of several key reproductive states including type of parental care (maternal, paternal, or biparental), internal versus external fertilization, internal versus external gestation, nest construction behavior, and presence versus absence of sexual dichromatism (as an indicator of sexual selection). Using a comparative phylogenetic approach, we critically evaluate several hypotheses regarding evolutionary pathways toward parental care. Results from maximum parsimony reconstructions indicate that all forms of parental care, including paternal, biparental, and maternal (both external and internal to the female reproductive tract) have arisen repeatedly and independently during ray‐finned fish evolution. The most common evolutionary transitions were from external fertilization directly to paternal care and from external fertilization to maternal care via the intermediate step of internal fertilization. We also used maximum likelihood phylogenetic methods to test for statistical correlations and contingencies in the evolution of pairs of reproductive traits. Sexual dichromatism and nest construction proved to be positively correlated with the evolution of male parental care in species with external fertilization. Sexual dichromatism was also positively correlated with female‐internal fertilization and gestation. No clear indication emerged that female‐only care or biparental care were evolutionary outgrowths of male‐only care, or that biparental care has been a common evolutionary stepping stone between paternal and maternal care. Results are discussed in the context of prior thought about the evolution of alternative parental care modes in vertebrates.

The W, X, Y and Z of sex-chromosome dosage compensation

In species with highly differentiated sex chromosomes, imbalances in gene dosage between the sexes can affect overall organismal fitness. Regulatory mechanisms were discovered in several unrelated animals, which counter gene-dose differences between females and males, and these early findings suggested that dosage-compensating mechanisms were required for sex-chromosome evolution. However, recent reports in birds and moths contradict this view because these animals locally compensate only a few genes on the sex chromosomes, leaving the majority with different expression levels in males and females. These findings warrant a re-examination of the evolutionary forces underlying dosage compensation.

Pleiotropic Constraint Hampers the Resolution of Sexual Antagonism in Vertebrate Gene Expression

The numerous physiological and phenotypic differences between the sexes, as well as the disparity between male and female reproductive interests, result in sexual conflicts, which are often manifested at the genomic level. Sexually antagonistic genes benefit one sex at the expense of the other and experience strong pressure to evolve male‐ and female‐specific expression patterns to resolve sexual conflicts and maximize fitness for both sexes. Sex‐biased gene expression has recently been demonstrated for much of the metazoan transcriptome, suggesting that many loci are sexually antagonistic. However, many coding regions function in multiple processes throughout the organism. This pleiotropy increases the complexity of selection for any given gene, which in turn may obscure sex‐specific selective pressures and hamper the evolution of sex‐biased gene expression. Here we use microarray gene expression data, in conjunction with data on transcript abundance from expressed sequence tag libraries, to demonstrate that loci with sex‐biased gene expression are significantly less pleiotropic than unbiased genes. This relationship was independent of sex chromosome gene dosage effects, and the results were concordant across two study organisms, chicken and mouse. These results suggest that the resolution of sexually antagonistic gene expression is determined by the evolutionary constraints acting on any given antagonistic locus.

All dosage compensation is local: Gene-by-gene regulation of sex-biased expression on the chicken Z chromosome

Recent reports have suggested that birds lack a mechanism of wholesale dosage compensation for the Z sex chromosome. This discovery was rather unexpected, as all other animals investigated with chromosomal mechanisms of sex determination have some method to counteract the effects of gene dosage of the dominant sex chromosome in males and females. Despite the lack of a global mechanism of avian dosage compensation, the pattern of gene expression difference between males and females varies a great deal for individual Z-linked genes. This suggests that some genes may be individually dosage compensated, and that some less-than-global pattern of dosage compensation, such as local or temporal, exists on the avian Z chromosome. We used global gene expression profiling in males and females for both somatic and gonadal tissue at several time points in the life cycle of the chicken to assess the pattern of sex-biased gene expression on the Z chromosome. Average fold-change between males and females varied somewhat among tissue time-point combinations, with embryonic brain samples having the smallest gene dosage effects, and adult gonadal tissue having the largest degree of male bias. Overall, there were no neighborhoods of overall dosage compensation along the Z. Taken together, this suggests that dosage compensation is regulated on the Z chromosome entirely on a gene-by-gene level, and can vary during the life cycle and by tissue type. This regulation may be an indication of how critical a given genes functionality is, as the expression level for essential genes will be tightly regulated in order to avoid perturbing important pathways and networks with differential expression levels in males and females.

Evolutionary Diversity and Turn-Over of Sex Determination in Teleost Fishes

Sex determination, due to the obvious association with reproduction and Darwinian fitness, has been traditionally assumed to be a relatively conserved trait. However, research on teleost fishes has shown that this need not be the case, as these animals display a remarkable diversity in the ways that they determine sex. These different mechanisms, which include constitutive genetic mechanisms on sex chromosomes, polygenic constitutive mechanisms, environmental influences, hermaphroditism, and unisexuality have each originated numerous independent times in the teleosts. The evolutionary lability of sex determination, and the corresponding rapid rate of turn-over among different modes, makes the teleost clade an excellent model with which to test theories regarding the evolution of sex determining adaptations. Much of the plasticity in sex determination likely results from the dynamic teleost genome, and recent advances in fish genetics and genomics have revealed the role of gene and genome duplication in fostering emergence and turn-over of sex determining mechanisms.