Evolution and conservation of Characidium sex chromosomes.

Fish species exhibit substantial variation in the degree of genetic differentiation between sex chromosome pairs, and therefore offer the opportunity to study the full range of sex chromosome evolution. We used restriction-site associated DNA sequencing (RAD-seq) to study the sex chromosomes of Characidium gomesi, a species with conspicuous heteromorphic ZW/ZZ sex chromosomes. We screened 9863 single-nucleotide polymorphisms (SNPs), corresponding to ~1 marker/100 kb distributed across the genome for sex-linked variation. With this data set, we identified 26 female-specific RAD loci, putatively located on the W chromosome, as well as 148 sex-associated SNPs showing significant differentiation (average FST=0.144) between males and females, and therefore in regions of more recent divergence between the Z and W chromosomes. In addition, we detected 25 RAD loci showing extreme heterozygote deficiency in females but which were in Hardy-Weinberg equilibrium in males, consistent with degeneration of the W chromosome and therefore female hemizygosity. We validated seven female-specific and two sex-associated markers in a larger sample of C. gomesi, of which three localised to the W chromosome, thereby providing useful markers for sexing wild samples. Validated markers were evaluated in other populations and species of the genus Characidium, this exploration suggesting a rapid turnover of W-specific repetitive elements. Together, our analyses point to a complex origin for the sex chromosome of C. gomesi and highlight the utility of RAD-seq for studying the composition and evolution of sex chromosomes systems in wild populations.

The locus of sexual selection: moving sexual selection studies into the post-genomics era.

Sexual selection drives fundamental evolutionary processes such as trait elaboration and speciation. Despite this importance, there are surprisingly few examples of genes unequivocally responsible for variation in sexually selected phenotypes. This lack of information inhibits our ability to predict phenotypic change due to universal behaviours, such as fighting over mates and mate choice. Here, we discuss reasons for this apparent gap and provide recommendations for how it can be overcome by adopting contemporary genomic methods, exploiting underutilized taxa that may be ideal for detecting the effects of sexual selection and adopting appropriate experimental paradigms. Identifying genes that determine variation in sexually selected traits has the potential to improve theoretical models and reveal whether the genetic changes underlying phenotypic novelty utilize common or unique molecular mechanisms. Such a genomic approach to sexual selection will help answer questions in the evolution of sexually selected phenotypes that were first asked by Darwin and can furthermore serve as a model for the application of genomics in all areas of evolutionary biology.

The role of sex chromosomes in sexual dimorphism: discordance between molecular and phenotypic data.

In addition to initial sex determination, genes on the sex chromosomes are theorized to play a particularly important role in phenotypic differences between males and females. Sex chromosomes in many species display molecular signatures consistent with these theoretical predictions, particularly through sex-specific gene expression. However, the phenotypic implications of this molecular signature are unresolved, and the role of the sex chromosomes in quantitative genetic studies of phenotypic sex differences is largely equivocal. In this article, we examine molecular and phenotypic data in the light of theoretical predictions about masculinization and feminization of the sex chromosomes. Additionally, we discuss the role of genetic and regulatory complexities in the genome­phenotype relationship, and ultimately how these affect the overall role of the sex chromosomes in sex differences.

The scope and strength of sex-specific selection in genome evolution.

Males and females share the vast majority of their genomes and yet are often subject to different, even conflicting, selection. Genomic and transcriptomic developments have made it possible to assess sex-specific selection at the molecular level, and it is clear that sex-specific selection shapes the evolutionary properties of several genomic characteristics, including transcription, post-transcriptional regulation, imprinting, genome structure and gene sequence. Sex-specific selection is strongly influenced by mating system, which also causes neutral evolutionary changes that affect different regions of the genome in different ways. Here, we synthesize theoretical and molecular work in order to provide a cohesive view of the role of sex-specific selection and mating system in genome evolution. We also highlight the need for a combined approach, incorporating both genomic data and experimental phenotypic studies, in order to understand precisely how sex-specific selection drives evolutionary change across the genome.

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.

Evolutionary perspectives on hermaphroditism in fishes.

Hermaphroditism is a derived and polyphyletic condition in fishes, documented in about 2% of all extant teleost species scattered across more than 20 taxonomic families in 9 orders. It shows a variety of expressions that can be categorized into sequential and synchronous modes. Among the sequential hermaphrodites are protogynous species in which an individual begins reproductive life as a female and later may switch to male, protandrous species in which a fish starts as a male and later may switch to female, and serial bi-directional sex changers. Among the synchronous hermaphrodites (in which an individual can simultaneously produce eggs and sperm) are several outcrossing and one predominantly selfing species. A few species also consist of mixtures of hermaphroditic and single-sex individuals. All of these reproductive categories have been the subject of numerous theoretical and empirical treatments from an evolutionary perspective. Here we highlight some of the major conclusions from these studies, which collectively have been informative on a variety of biological topics related to reproductive modes, gender allocations, sexual conflict and gamesmanship, mating systems, and life-history tradeoffs.

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 gene's 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.

Mating preferences, sexual selection and patterns of cladogenesis in ray-finned fishes.

Evolutionary theory predicts that sexual selection may increase taxonomic diversity when emergent mating preferences result in reproductive isolation and therefore speciation. This theory has been invoked to explain patterns of diversity in ray-finned fishes (most notably in the cichlids), but the theory has not been tested comparatively in fish. Additionally, several other unrelated factors have been identified as promoters of cladogenesis, so it is unclear how important sexual selection might be in diversification. Using sister-clade analysis, I tested the relationship between the presence of sexually selected traits and taxonomic diversification in actinopterygiian fishes, a large clade that shows substantial diversity in mating preferences and related sexually selected traits. In all identified sister-families that differed with regard to the proportion of species manifesting sexually selected traits, sexual selection was correlated with increased diversification, and this association was significant across all sister clades (P=0.02). This suggests that sexual selection, when present, is a substantial driver of diversification in the ray-finned fishes, and lends further empirical support to the theoretical link between mating preferences and accelerated cladogenesis.

Supertree analyses of the roles of viviparity and habitat in the evolution of atherinomorph fishes.

Using supertree phylogenetic reconstructions, we investigate how livebearing and freshwater adaptations may have shaped evolutionary patterns in the Atherinomorpha, a large clade (approximately 1500 extant species) of ray-finned fishes. Based on maximum parsimony reconstructions, livebearing appears to have evolved at least four times independently in this group, and no reversions to the ancestral state of oviparity were evident. With respect to habitat, at least five evolutionary transitions apparently occurred from freshwater to marine environments, at least two transitions in the opposite direction, and no clear ancestral state was identifiable. All viviparous clades exhibited more extant species than their oviparous sister taxa, suggesting that transitions to viviparity may be associated with cladogenetic diversification. Transitions to freshwater were usually, but not invariably associated with increased species richness, but the trend was, overall, not significant among sister clades. Additionally, we investigated whether livebearing and freshwater adaptations are currently associated with elevated risks of extinction as implied by species' presence on the 2004 IUCN Red List. Despite being correlated with decreased brood size, livebearing has not significantly increased extinction risk in the Atherinomorpha. However, freshwater species were significantly more likely than marine species to be listed as endangered.

Microsatellite variation and differentiation in North Atlantic eels.

We screened 11 populations of American, European, and Icelandic eels (Anguillidae) for allelic variation and genetic divergence at six polymorphic microsatellite loci. Within either of the two recognized Anguilla species in the North Atlantic (rostrata in the Americas, anguilla in Europe), population genetic structure was statistically significant but weak; fully 95% of the total genetic variation was present within geographic locales rather than distributed among them. The two Anguilla species also overlap greatly in allelic frequencies, so the available data proved ineffective for addressing hypotheses about the possible hybrid origins of some Icelandic eels. The overlapping microsatellite profiles contrast with nearly diagnostic species differences documented previously in allozymes and mtDNA. This and similar empirical findings in several other species support theoretical concerns that homoplasy (convergent evolution) in allelic states can compromise the utility of rapidly mutating microsatellite loci for certain types of microevolutionary questions regarding gene flow and species differences.