Molly Schumer

Parallel Molecular Evolution in an Herbivore Community

Making the Change The Apocynaceae plant family produces toxic cardenolids. However, many insects have managed to escape the deleterious effects of these chemicals and even, in some cases, use them in their own defense. Zhen et al. (p. 1634) investigated a broad range of taxa and found several examples of parallel changes, as well as duplications, in members of the ATPα family that likely explain the shift to allow insects to avoid the toxic effects of these plants. Thus, natural selection can harness a combination of gene duplication, protein evolution, and regulatory evolution to allow distantly related species to adapt to specific niches. Parallel mutations in the alpha subunit of the sodium pump allow insects to specialize on host plants that produce ouabain. Numerous insects have independently evolved the ability to feed on plants that produce toxic secondary compounds called cardenolides and can sequester these compounds for use in their defense. We surveyed the protein target for cardenolides, the alpha subunit of the sodium pump, Na+,K+-ATPase (ATPα), in 14 species that feed on cardenolide-producing plants and 15 outgroups spanning three insect orders. Despite the large number of potential targets for modulating cardenolide sensitivity, amino acid substitutions associated with host-plant specialization are highly clustered, with many parallel substitutions. Additionally, we document four independent duplications of ATPα with convergent tissue-specific expression patterns. We find that unique substitutions are disproportionately associated with recent duplications relative to parallel substitutions. Together, these findings support the hypothesis that adaptation tends to take evolutionary paths that minimize negative pleiotropy.

PHYLOGENOMICS REVEALS EXTENSIVE RETICULATE EVOLUTION IN XIPHOPHORUS FISHES

Hybridization is increasingly being recognized as a widespread process, even between ecologically and behaviorally divergent animal species. Determining phylogenetic relationships in the presence of hybridization remains a major challenge for evolutionary biologists, but advances in sequencing technology and phylogenetic techniques are beginning to address these challenges. Here we reconstruct evolutionary relationships among swordtails and platyfishes (Xiphophorus: Poeciliidae), a group of species characterized by remarkable morphological diversity and behavioral barriers to interspecific mating. Past attempts to reconstruct phylogenetic relationships within Xiphophorus have produced conflicting results. Because many of the 26 species in the genus are interfertile, these conflicts are likely due to hybridization. Using genomic data, we resolve a high‐confidence species tree of Xiphophorus that accounts for both incomplete lineage sorting and hybridization. Our results allow us to reexamine a long‐standing controversy about the evolution of the sexually selected sword in Xiphophorus, and demonstrate that hybridization has been strikingly widespread in the evolutionary history of this genus.

HOW COMMON IS HOMOPLOID HYBRID SPECIATION

Hybridization has long been considered a process that prevents divergence between species. In contrast to this historical view, an increasing number of empirical studies claim to show evidence for hybrid speciation without a ploidy change. However, the importance of hybridization as a route to speciation is poorly understood, and many claims have been made with insufficient evidence that hybridization played a role in the speciation process. We propose criteria to determine the strength of evidence for homoploid hybrid speciation. Based on an evaluation of the literature using this framework, we conclude that although hybridization appears to be common, evidence for an important role of hybridization in homoploid speciation is more circumscribed.

A serine cluster mediates BMAL1-dependent CLOCK phosphorylation and degradation

The circadian clock regulates biological processes from gene expression to organism behavior in a precise, sustained rhythm that is generated at the unicellular level by coordinated function of interlocked transcriptional feedback loops and post-translational modifications of core clock proteins. CLOCK phosphorylation regulates transcriptional activity, cellular localization and stability; however little is known about the specific residues and enzymes involved. We have identified a conserved cluster of serines that include, Ser431, which is a prerequisite phosphorylation site for the generation of BMAL dependent phospho-primed CLOCK and for the potential GSK-3 phosphorylation at Ser427. Mutational analysis and protein stability assays indicate that this serine cluster functions as a phospho-degron. Through the use of GSK-3 activators/inhibitors and kinase assays, we demonstrate that GSK-3β regulates the degron-site by increasing CLOCK phosphorylation/degradation, which correlates with an increase in the expression of CLOCK responsive promoters. Stabilization of phospho-deficient CLOCK delays the phase of oscillation in synchronized fibroblasts. This investigation begins the characterization of a complex phospho-regulatory site that controls the degradation of CLOCK, a core transcription factor that is essential for circadian behavior.

Genetic accommodation and behavioural evolution: insights from genomic studies

Many behaviours vary in response to the environment (biotic or abiotic) and therefore represent an interesting form of phenotypic plasticity. Behavioural plasticity, like other plastic traits, can evolve through genetic assimilation or accommodation. However, little is known about the nature of changes in gene expression plasticity that accompanies these evolutionary changes in phenotypic plasticity. We know that variation in gene expression level, a first-order phenotype, underlies much behavioural variation. Several studies have begun to document which genes show expression-level variation related to plastic changes in behaviour as well as evolved changes in behaviour. Advances in sequencing technology allow us to address these questions on a genomic scale. By characterizing changes in gene expression according to the concept of a norm of reaction one can describe the evolved patterns of gene expression that accompany the evolution of behavioural plasticity. Here, we describe how genomic approaches can help us understand changes in gene expression that accompany or underlie the evolution of behavioural plasticity. To do this, we provide a framework of classification for the evolved patterns of gene expression plasticity that could underlie genetic assimilation or accommodation of behaviour. We provide examples of genetic assimilation from the animal behaviour and animal physiology literature that have been, or can be, studied at a genomic level. We then describe the characteristics of an appropriate study system and briefly address experimental design using the available genomic tools in a comparative context. Studying the patterns of gene expression associated with genetic assimilation will elucidate processes by which behavioural plasticity has evolved.

High-resolution mapping reveals hundreds of genetic incompatibilities in hybridizing fish species

Hybridization is increasingly being recognized as a common process in both animal and plant species. Negative epistatic interactions between genes from different parental genomes decrease the fitness of hybrids and can limit gene flow between species. However, little is known about the number and genome-wide distribution of genetic incompatibilities separating species. To detect interacting genes, we perform a high-resolution genome scan for linkage disequilibrium between unlinked genomic regions in naturally occurring hybrid populations of swordtail fish. We estimate that hundreds of pairs of genomic regions contribute to reproductive isolation between these species, despite them being recently diverged. Many of these incompatibilities are likely the result of natural or sexual selection on hybrids, since intrinsic isolation is known to be weak. Patterns of genomic divergence at these regions imply that genetic incompatibilities play a significant role in limiting gene flow even in young species. DOI: http://dx.doi.org/10.7554/eLife.02535.001

Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities

Despite its role in homogenizing populations, hybridization has also been proposed as a means to generate new species. The conceptual basis for this idea is that hybridization can result in novel phenotypes through recombination between the parental genomes, allowing a hybrid population to occupy ecological niches unavailable to parental species. Here we present an alternative model of the evolution of reproductive isolation in hybrid populations that occurs as a simple consequence of selection against genetic incompatibilities. Unlike previous models of hybrid speciation, our model does not incorporate inbreeding, or assume that hybrids have an ecological or reproductive fitness advantage relative to parental populations. We show that reproductive isolation between hybrids and parental species can evolve frequently and rapidly under this model, even in the presence of substantial ongoing immigration from parental species and strong selection against hybrids. An interesting prediction of our model is that replicate hybrid populations formed from the same pair of parental species can evolve reproductive isolation from each other. This non-adaptive process can therefore generate patterns of species diversity and relatedness that resemble an adaptive radiation. Intriguingly, several known hybrid species exhibit patterns of reproductive isolation consistent with the predictions of our model.

Repeated losses of PRDM9-directed recombination despite the conservation of PRDM9 across vertebrates

Studies of highly diverged species have revealed two mechanisms by which meiotic recombination is directed to the genome—through PRDM9 binding or by targeting promoter-like features—that lead to dramatically different evolutionary dynamics of hotspots. Here, we identify PRDM9 orthologs from genome and transcriptome data in 225 species. We find the complete PRDM9 ortholog across distantly related vertebrates but, despite this broad conservation, infer a minimum of six partial and three complete losses. Strikingly, taxa carrying the complete ortholog of PRDM9 are precisely those with rapid evolution of its predicted binding affinity, suggesting that all domains are necessary for directing recombination. Indeed, as we show, swordtail fish carrying only a partial but conserved ortholog share recombination properties with PRDM9 knock-outs. DOI: http://dx.doi.org/10.7554/eLife.24133.001

An evaluation of the hybrid speciation hypothesis for Xiphophorus clemenciae based on whole genome sequences.

Once thought rare in animal taxa, hybridization has been increasingly recognized as an important and common force in animal evolution. In the past decade, a number of studies have suggested that hybridization has driven speciation in some animal groups. We investigate the signature of hybridization in the genome of a putative hybrid species, Xiphophorus clemenciae, through whole genome sequencing of this species and its hypothesized progenitors. Based on analysis of this data, we find that X. clemenciae is unlikely to have been derived from admixture between its proposed parental species. However, we find significant evidence for recent gene flow between Xiphophorus species. Although we detect genetic exchange in two pairs of species analyzed, the proportion of genomic regions that can be attributed to hybrid origin is small, suggesting that strong behavioral premating isolation prevents frequent hybridization in Xiphophorus. The direction of gene flow between species is potentially consistent with a role for sexual selection in mediating hybridization.

Comparative gene expression profiles for highly similar aggressive phenotypes in male and female cichlid fishes (Julidochromis)

SUMMARY Julidochromis marlieri and Julidochromis transcriptus are two closely related Tanganyikan cichlids that have evolved different behavior and mating strategies since they diverged from their common ancestor. While J. transcriptus follows the ancestral pattern of male dominance, male-biased sexual size dimorphism and territoriality, the pattern is reversed in J. marlieri. In J. marlieri, females show all of these behavioral and morphological characteristics. This raises the question of whether female J. marlieri achieve the dominant phenotype by expressing the same genes as J. transcriptus males or whether novel brain gene expression patterns have evolved to produce a similar behavioral phenotype in the females of J. marlieri. This study used cDNA microarrays to investigate whether female J. marlieri and male J. transcriptus show conserved or divergent patterns of brain gene expression. Analysis of microarray data in both species showed certain gene expression patterns associated with sex role independent of gonadal sex and, to a lesser extent, gene expression patterns associated with sex independent of sex role. In general, these data suggest that while there has been substantial divergence in gene expression patterns between J. transcriptus and J. marlieri, we can detect a highly significant overlap for a core set of genes related to aggression in both species. These results suggest that the proximate mechanisms regulating aggressive behavior in J. transcriptus and J. marlieri may be shared.