Vera B. Kaiser

Out of the Andes: patterns of diversification in clearwing butterflies

Global biodiversity peaks in the tropical forests of the Andes, a striking geological feature that has likely been instrumental in generating biodiversity by providing opportunities for both vicariant and ecological speciation. However, the role of these mountains in the diversification of insects, which dominate biodiversity, has been poorly explored using phylogenetic methods. Here we study the role of the Andes in the evolution of a diverse Neotropical insect group, the clearwing butterflies. We used dated species‐level phylogenies to investigate the time course of speciation and to infer ancestral elevation ranges for two diverse genera. We show that both genera likely originated at middle elevations in the Andes in the Middle Miocene, contrasting with most published results in vertebrates that point to a lowland origin. Although we detected a signature of vicariance caused by the uplift of the Andes at the Miocene–Pliocene boundary, most sister species were parapatric without any obvious vicariant barrier. Combined with an overall decelerating speciation rate, these results suggest an important role for ecological speciation and adaptive radiation, rather than simple vicariance.

The effects of deleterious mutations on evolution in non-recombining genomes

Analyzing regions of the Drosophila genome that have low levels of genetic recombination helps us understand the prevalence of sexual reproduction. Here, we show that genetic variability in these regions can be explained by interference among strongly deleterious mutations and that selection becomes progressively less effective in influencing the behaviour of neighbouring sites as the number of closely linked sites on a chromosome increases.

Evolution of Sex Chromosomes in Insects

Sex chromosomes have many unusual features relative to autosomes. Y (or W) chromosomes lack genetic recombination, are male- (female-) limited, and show an abundance of genetically inert heterochromatic DNA but contain few functional genes. X (or Z) chromosomes also show sex-biased transmission (i.e., X chromosomes show female-biased and Z-chromosomes show male-biased inheritance) and are hemizygous in the heterogametic sex. Their unusual ploidy level and pattern of inheritance imply that sex chromosomes play a unique role in many biological processes and phenomena, including sex determination, epigenetic chromosome-wide regulation of gene expression, the distribution of genes in the genome, genomic conflict, local adaptation, and speciation. The vast diversity of sex chromosome systems in insects--ranging from the classical male heterogametic XY system in Drosophila to ZW systems in Lepidoptera or mobile genes determining sex as found in house flies--implies that insects can serve as unique model systems to study various functional and evolutionary aspects of these different processes.

Sex-biased gene expression at homomorphic sex chromosomes in emus and its implication for sex chromosome evolution

Sex chromosomes originate from autosomes. The accumulation of sexually antagonistic mutations on protosex chromosomes selects for a loss of recombination and sets in motion the evolutionary processes generating heteromorphic sex chromosomes. Recombination suppression and differentiation are generally viewed as the default path of sex chromosome evolution, and the occurrence of old, homomorphic sex chromosomes, such as those of ratite birds, has remained a mystery. Here, we analyze the genome and transcriptome of emu (Dromaius novaehollandiae) and confirm that most genes on the sex chromosome are shared between the Z and W. Surprisingly, however, levels of gene expression are generally sex-biased for all sex-linked genes relative to autosomes, including those in the pseudoautosomal region, and the male-bias increases after gonad formation. This expression bias suggests that the emu sex chromosomes have become masculinized, even in the absence of ZW differentiation. Thus, birds may have taken different evolutionary solutions to minimize the deleterious effects imposed by sexually antagonistic mutations: some lineages eliminate recombination along the protosex chromosomes to physically restrict sexually antagonistic alleles to one sex, whereas ratites evolved sex-biased expression to confine the product of a sexually antagonistic allele to the sex it benefits. This difference in conflict resolution may explain the preservation of recombining, homomorphic sex chromosomes in other lineages and illustrates the importance of sexually antagonistic mutations driving the evolution of sex chromosomes.

Genetic Recombination and Molecular Evolution

Reduced rates of genetic recombination are often associated with reduced genetic variability and levels of adaptation. Several different evolutionary processes, collectively known as Hill-Robertson (HR) effects, have been proposed as causes of these correlates of recombination. Here, we use DNA sequence polymorphism and divergence data from the noncrossing over dot chromosome of Drosophila to discriminate between two of the major forms of HR effects: selective sweeps and background selection. This chromosome shows reduced levels of silent variability and reduced effectiveness of selection. We show that neither model fits the data on variability. We propose that, in large genomic regions with restricted recombination, HR effects among nonsynonymous mutations undermine the effective strength of selection, so that their background selection effects are weakened. This modified model fits the data on variability and also explains why variability in very large nonrecombining genomes is not completely wiped out. We also show that HR effects of this type can produce an individual selection advantage to recombination, as well as greatly reduce the mean fitness of nonrecombining genomes and genomic regions.

NONRANDOM DISTRIBUTION OF GENES WITH SEX-BIASED EXPRESSION IN THE CHICKEN GENOME

Abstract Evolutionary theory predicts that sexually antagonistic genes should show a nonrandom genomic distribution with sex chromosomes usually being enriched for such genes. However, empirical observations from model organisms (Drosophila melanogaster, Caenorhabditis elegans, mammals) on the genomic location of genes with sex-biased expression have provided conflicting data and are not easily explained by a unified framework based on standard models of the evolution of sexually antagonistic genes. Previous studies have been confined to organisms with male heterogamety, meaning that effects related to homo- or heterozygosity of sex chromosomes cannot be separated from effects related to sex-specific characteristics. We therefore studied the genomic distribution of genes with sex-biased expression in the chicken, that is, in an organism with female heterogamety (males ZZ, females ZW). From the abundance of transcripts in expressed sequence tag libraries, we found an underrepresentation of female-specific genes (germ line and somatic tissue) and an overrepresentation of male-specific genes (somatic) on the Z chromosome. This is consistent with theoretical predictions only if mutations beneficial to one sex generally tend to be at least partly dominant (h > 0.5). We also note that sexual selection for a male-biased trait is facilitated by Z-linkage, because sons in organisms with female heterogamety will always inherit a Z chromosome from their fathers.

The Epigenome of Evolving Drosophila Neo-Sex Chromosomes: Dosage Compensation and Heterochromatin Formation

This study shows how young sex chromosomes have altered their chromatin structure in Drosophila, and what genomic changes have led to silencing of the Y, and hyper-transcription of the X.

Muller's Ratchet and the Degeneration of the Drosophila miranda Neo-Y Chromosome

Since its formation about 1.75 million years ago, the Drosophila miranda neo-Y chromosome has undergone a rapid process of degeneration, having lost approximately half of the genes that it originally contained. Using estimates of mutation rates and selection coefficients for loss-of-function mutations, we show that the high rate of accumulation of these mutations can largely be explained by Mullers ratchet, the process of stochastic loss of the least-loaded mutational class from a finite, nonrecombining population. We show that selection at nonsynonymous coding sites can accelerate the process of gene loss and that this effect varies with the number of genes still present on the degenerating neo-Y chromosome.

Conservation and de novo acquisition of dosage compensation on newly evolved sex chromosomes in Drosophila

Dosage compensation has arisen in response to the evolution of distinct male (XY) and female (XX) karyotypes. In Drosophila melanogaster, the MSL complex increases male X transcription approximately twofold. X-specific targeting is thought to occur through sequence-dependent binding to chromatin entry sites (CESs), followed by spreading in cis to active genes. We tested this model by asking how newly evolving sex chromosome arms in Drosophila miranda acquired dosage compensation. We found evidence for the creation of new CESs, with the analogous sequence and spacing as in D. melanogaster, providing strong support for the spreading model in the establishment of dosage compensation.

Nonrandom Gene Loss from the Drosophila miranda Neo-Y Chromosome

A lack of recombination leads to the degeneration of an evolving Y chromosome. However, it is not known whether gene loss is largely a random process and primarily driven by the order in which mutations occur or whether certain categories of genes are lost less quickly than others; the latter would imply that selection counteracts the degeneration of Y chromosomes to some extent. In this study, we investigate the relationship between putative ancestral expression levels of neo-Y–linked genes in Drosophila miranda and their rates of degeneration. We use RNA-Seq data from its close relative Drosophila pseudoobscura to show that genes that have become nonfunctional on the D. miranda neo-Y had, on average, lower ancestral transcript levels and were expressed in fewer tissues compared with genes with intact reading frames. We also show that genes with male-biased expression are retained for longer on the neo-Y compared with female-biased genes. Our results imply that gene loss on the neo-Y is not a purely random, mutation-driven process. Instead, selection is—at least to some extent—preserving the function of genes that are more costly to lose, despite the strongly reduced efficacy of selection on the neo-Y chromosome.