Doris Bachtrog

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.

Horizontal Gene Transfer from Diverse Bacteria to an Insect Genome Enables a Tripartite Nested Mealybug Symbiosis

The smallest reported bacterial genome belongs to Tremblaya princeps, a symbiont of Planococcus citri mealybugs (PCIT). Tremblaya PCIT not only has a 139 kb genome, but possesses its own bacterial endosymbiont, Moranella endobia. Genome and transcriptome sequencing, including genome sequencing from a Tremblaya lineage lacking intracellular bacteria, reveals that the extreme genomic degeneracy of Tremblaya PCIT likely resulted from acquiring Moranella as an endosymbiont. In addition, at least 22 expressed horizontally transferred genes from multiple diverse bacteria to the mealybug genome likely complement missing symbiont genes. However, none of these horizontally transferred genes are from Tremblaya, showing that genome reduction in this symbiont has not been enabled by gene transfer to the host nucleus. Our results thus indicate that the functioning of this three-way symbiosis is dependent on genes from at least six lineages of organisms and reveal a path to intimate endosymbiosis distinct from that followed by organelles.

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.

EXTENSIVE INTROGRESSION OF MITOCHONDRIAL DNA RELATIVE TO NUCLEAR GENES IN THE DROSOPHILA YAKUBA SPECIES GROUP

Abstract Studies of gene flow between recently diverged species can illuminate the role of natural selection in the formation of new species. Drosophila santomea and D. yakuba are recently diverged, partially reproductively isolated species that continue to hybridize in the wild, and appear to be reproductively isolated from the more distantly related species D. teissieri. We examine patterns of nucleotide polymorphism and divergence in these three species at multiple X‐linked, Y‐linked, and mitochondrial markers. All three species harbor drastically reduced variability on the Y chromosome relative to the X, as expected for a nonrecombining chromosome subject to variation‐reducing selection. The three species are generally well differentiated at the nuclear markers, with little evidence for recent introgression for either the X‐ or Y‐linked genes. Based on the nuclear genes, we estimate that D. santomea and D. yakuba diverged about one‐half million years ago and split from D. teissieri about one million years ago. In contrast to the pattern at nuclear loci, all three species share a very similar mtDNA haplotype. We show that the mtDNA must have recently introgressed across species boundaries in the D. yakuba subgroup and that its fixation was driven by either selection on the mitochondria itself or other cytoplasmic factors. These results demonstrate that different regions of the genome can have distinct evolutionary dynamics in the context of species formation. Although natural selection is usually thought of as accentuating divergence between species, our results imply that it can also act as a homogenizing force

Comparative Sex Chromosome Genomics in Snakes: Differentiation, Evolutionary Strata, and Lack of Global Dosage Compensation

Analysis of the genomes and transcriptomes of snake species with homomorphic and heteromorphic sex chromosomes reveals the evolutionary dynamics of sex chromosome differentiation.

Genomic degradation of a young Y chromosome in Drosophila miranda.

BackgroundY chromosomes are derived from ordinary autosomes and degenerate because of a lack of recombination. Well-studied Y chromosomes only have few of their original genes left and contain little information about their evolutionary origin. Here, we take advantage of the recently formed neo-Y chromosome of Drosophila miranda to study the processes involved in Y degeneration on a genomic scale.ResultsWe obtained sequence information from 14 homologous bacterial artificial chromosome (BAC) clones from the neo-X and neo-Y chromosome of D. miranda, encompassing over 2.5 Mb of neo-sex-linked DNA. A large fraction of neo-Y DNA is composed of repetitive and transposable-element-derived DNA (20% of total DNA) relative to their homologous neo-X linked regions (1%). The overlapping regions of the neo-sex linked BAC clones contain 118 gene pairs, half of which are pseudogenized on the neo-Y. Pseudogenes evolve significantly faster on the neo-Y than functional genes, and both functional and non-functional genes show higher rates of protein evolution on the neo-Y relative to their neo-X homologs. No heterogeneity in levels of degeneration was detected among the regions investigated. Functional genes on the neo-Y are under stronger evolutionary constraint on the neo-X, but genes were found to degenerate randomly on the neo-Y with regards to their function or sex-biased expression patterns.ConclusionPatterns of genome evolution in D. miranda demonstrate that degeneration of a recently formed Y chromosome can proceed very rapidly, by both an accumulation of repetitive DNA and degeneration of protein-coding genes. Our data support a random model of Y inactivation, with little heterogeneity in degeneration among genomic regions, or between functional classes of genes or genes with sex-biased expression patterns.

The Temporal Dynamics of Processes Underlying Y Chromosome Degeneration

Y chromosomes originate from ordinary autosomes and degenerate by accumulating deleterious mutations. This accumulation results from a lack of recombination on the Y and is driven by interference among deleterious mutations (Mullers ratchet and background selection) and the fixation of beneficial alleles (genetic hitchhiking). Here I show that the relative importance of these processes is expected to vary over the course of Y chromosome evolution due to changes in the number of active genes. The dominant mode of degeneration on a newly formed gene-rich Y chromosome is expected to be Mullers ratchet and/or background selection due to the large numbers of deleterious mutations arising in active genes. However, the relative importance of these modes of degeneration declines rapidly as active genes are lost. In contrast, the rate of degeneration due to hitchhiking is predicted to be highest on Y chromosomes containing an intermediate number of active genes. The temporal dynamics of these processes imply that a gradual restriction of recombination, as inferred in mammals, will increase the importance of genetic hitchhiking relative to Mullers ratchet and background selection.

Sex-Biased Transcriptome Evolution in Drosophila

Sex-biased genes are thought to drive phenotypic differences between males and females. The recent availability of high-throughput gene expression data for many related species has led to a burst of investigations into the genomic and evolutionary properties of sex-biased genes. In Drosophila, a number of studies have found that X chromosomes are deficient in male-biased genes (demasculinized) and enriched for female-biased genes (feminized) and that male-biased genes evolve faster than female-biased genes. However, studies have yielded vastly different conclusions regarding the numbers of sex-biased genes and forces shaping their evolution. Here, we use RNA-seq data from multiple tissues of Drosophila melanogaster and D. pseudoobscura, a species with a recently evolved X chromosome, to explore the evolution of sex-biased genes in Drosophila. First, we compare several independent metrics for classifying sex-biased genes and find that the overlap of genes identified by different metrics is small, particularly for female-biased genes. Second, we investigate genome-wide expression patterns and uncover evidence of demasculinization and feminization of both ancestral and new X chromosomes, demonstrating that gene content on sex chromosomes evolves rapidly. Third, we examine the evolutionary rates of sex-biased genes and show that male-biased genes evolve much faster than female-biased genes, which evolve at similar rates to unbiased genes. Analysis of gene expression among tissues reveals that this trend may be partially due to pleiotropic effects of female-biased genes, which limits their evolutionary potential. Thus, our findings illustrate the importance of accurately identifying sex-biased genes and provide insight into their evolutionary dynamics in Drosophila.

Sex-specific adaptation drives early sex chromosome evolution in Drosophila.

Sex Chromosome Evolution The fly genus Drosophilia has repeatedly generated evolutionarily new sex chromosomes. To understand the changes shaping the X and Y chromosomes, Zhou and Bachtrog (p. 341), sequenced the genome of D. miranda, which formed neo-X and neo-Y chromosomes approximately 1 million years ago. The data illuminate the ongoing conflict between selection for male and female function on the sex chromosomes and show that Y chromosome evolution is characterized both by a loss of gene function and selection for male-specific adaptations in genes beneficial to male functions. Evolutionarily new X and Y chromosomes evidence how selection for sexual function shapes sex chromosomes. Most species’ sex chromosomes are derived from ancient autosomes and show few signatures of their origins. We studied the sex chromosomes of Drosophila miranda, where a neo-Y chromosome originated only approximately 1 million years ago. Whole-genome and transcriptome analysis reveals massive degeneration of the neo-Y, that male-beneficial genes on the neo-Y are more likely to undergo accelerated protein evolution, and that neo-Y genes evolve biased expression toward male-specific tissues—the shrinking gene content of the neo-Y becomes masculinized. In contrast, although older X chromosomes show a paucity of genes expressed in male tissues, neo-X genes highly expressed in male-specific tissues undergo increased rates of protein evolution if haploid in males. Thus, the response to sex-specific selection can shift at different stages of X differentiation, resulting in masculinization or demasculinization of the X-chromosomal gene content.

Positive and Negative Selection on Noncoding DNA in Drosophila simulans

There is now a wealth of evidence that some of the most important regions of the genome are found outside those that encode proteins, and noncoding regions of the genome have been shown to be subject to substantial levels of selective constraint, particularly in Drosophila. Recent work has suggested that these regions may also have been subject to the action of positive selection, with large fractions of noncoding divergence having been driven to fixation by adaptive evolution. However, this work has focused on Drosophila melanogaster, which is thought to have experienced a reduction in effective population size (N(e)), and thus a reduction in the efficacy of selection, compared with its closest relative Drosophila simulans. Here, we examine patterns of evolution at several classes of noncoding DNA in D. simulans and find that all noncoding DNA is subject to the action of negative selection, indicated by reduced levels of polymorphism and divergence and a skew in the frequency spectrum toward rare variants. We find that the signature of negative selection on noncoding DNA and nonsynonymous sites is obscured to some extent by purifying selection acting on preferred to unpreferred synonymous codon mutations. We investigate the extent to which divergence in noncoding DNA is inferred to be the product of positive selection and to what extent these inferences depend on selection on synonymous sites and demography. Based on patterns of polymorphism and divergence for different classes of synonymous substitution, we find the divergence excess inferred in noncoding DNA and nonsynonymous sites in the D. simulans lineage difficult to reconcile with demographic explanations.