Several recent studies have estimated that a large fraction of amino acid divergence between species of Drosophila was fixed by positive selection, using statistical approaches based on the ...McDonald-Kreitman test. However, little is known about associated selection coefficients of beneficial amino acid mutations. Recurrent selective sweeps associated with adaptive substitutions should leave a characteristic signature in genome variability data that contains information about the frequency and strength of selection. Here, I document a significant negative correlation between the level and the frequency of synonymous site polymorphism and the rate of protein evolution in highly recombining regions of the X chromosome of D. melanogaster. This pattern is predicted by recurrent adaptive protein evolution and suggests that adaptation is an important determinant of patterns of neutral variation genome-wide. Using a maximum likelihood approach, I estimate the product of the rate and strength of selection under a recurrent genetic hitchhiking model, lambda2N(e)s approximately 3 x 10(-8). Using an approach based on the McDonald-Kreitman test, I estimate that approximately 50% of divergent amino acids were driven to fixation by positive selection, implying that beneficial amino acid substitutions are of weak effect on average, on the order of 10(-5) (i.e., 2N(e)s approximately 40). Two implications of these results are that most adaptive substitutions will be difficult to detect in genome scans of selection and that population size (and genetic drift) may be an important determinant of the evolutionary dynamics of protein adaptation.
The domesticated silkworm, Bombyx mori, and its wild progenitor, B. mandarina, are extensively studied as a model case of the evolutionary process of domestication. A conspicuous difference between ...these species is the dramatic reduction in melanin pigmentation in both larval and adult B. mori. Here we evaluate the efficiency of CRISPR/Cas9‐targeted knockouts of pigment‐related genes as a tool to understand their potential contributions to domestication‐associated melanin pigmentation loss in B. mori. To demonstrate the efficacy of targeted knockouts in B. mandarina, we generated a homozygous CRISPR/Cas9‐targeted knockout of yellow‐y. In yellow‐y knockout mutants, black body colour became lighter throughout the larval, pupal and adult stages, confirming a role for this gene in melanin pigment formation. Further, we performed allele‐specific CRISPR/Cas9‐targeted knockouts of the pigment‐related transcription factor, apontic‐like (apt‐like) in B. mori × B. mandarina F1 hybrid individuals which exhibit B. mandarina‐like larval pigmentation. Knockout of the B. mandarina allele of apt‐like in F1 embryos results in white patches on the dorsal integument of larvae, whereas corresponding knockouts of the B. mori allele consistently exhibit normal F1 larval pigmentation. These results demonstrate a contribution of apt‐like to the evolution of reduced melanin pigmentation in B. mori. Together, our results demonstrate the feasibility of CRISPR/Cas9‐targeted knockouts as a tool for understanding the genetic basis of traits associated with B. mori domestication.
Bombyx mori and its wild progenitor are an important model for the study of phenotypic evolution associated with domestication. As proof‐of‐principle, we used CRISPR/Cas9 to generate knockouts of two melanin pigmentation‐related genes. By generating a homozygous knockout of yellow‐y in B. mandarina, we confirmed this gene's role in melanin pigment formation. Further, by generating allele‐specific knockouts of apontic‐like in B. mori × B. mandarina F1 hybrids, we establish that evolution of apt‐like contributed to reduced melanin pigmentation during domestication.
We present a new approach to genotyping based on multiplexed shotgun sequencing that can identify recombination breakpoints in a large number of individuals simultaneously at a resolution sufficient ...for most mapping purposes, such as quantitative trait locus (QTL) mapping and mapping of induced mutations. We first describe a simple library construction protocol that uses just 10 ng of genomic DNA per individual and makes the approach accessible to any laboratory with standard molecular biology equipment. Sequencing this library results in a large number of sequence reads widely distributed across the genomes of multiplexed bar-coded individuals. We develop a Hidden Markov Model to estimate ancestry at all genomic locations in all individuals using these data. We demonstrate the utility of the approach by mapping a dominant marker allele in D. simulans to within 105 kb of its true position using 96 F1-backcross individuals genotyped in a single lane on an Illumina Genome Analyzer. We further demonstrate the utility of our method by genetically mapping more than 400 previously unassembled D. simulans contigs to linkage groups and by evaluating the quality of targeted introgression lines. At this level of multiplexing and divergence between strains, our method allows estimation of recombination breakpoints to a median of 38-kb intervals. Our analysis suggests that higher levels of multiplexing and/or use of strains with lower levels of divergence are practicable.
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.
Natural selection at one site shapes patterns of genetic variation at linked sites. Quantifying the effects of "linked selection" on levels of genetic diversity is key to making reliable inference ...about demography, building a null model in scans for targets of adaptation, and learning about the dynamics of natural selection. Here, we introduce the first method that jointly infers parameters of distinct modes of linked selection, notably background selection and selective sweeps, from genome-wide diversity data, functional annotations and genetic maps. The central idea is to calculate the probability that a neutral site is polymorphic given local annotations, substitution patterns, and recombination rates. Information is then combined across sites and samples using composite likelihood in order to estimate genome-wide parameters of distinct modes of selection. In addition to parameter estimation, this approach yields a map of the expected neutral diversity levels along the genome. To illustrate the utility of our approach, we apply it to genome-wide resequencing data from 125 lines in Drosophila melanogaster and reliably predict diversity levels at the 1Mb scale. Our results corroborate estimates of a high fraction of beneficial substitutions in proteins and untranslated regions (UTR). They allow us to distinguish between the contribution of sweeps and other modes of selection around amino acid substitutions and to uncover evidence for pervasive sweeps in untranslated regions (UTRs). Our inference further suggests a substantial effect of other modes of linked selection and of adaptation in particular. More generally, we demonstrate that linked selection has had a larger effect in reducing diversity levels and increasing their variance in D. melanogaster than previously appreciated.
Understanding why some species have more genetic diversity than others is central to the study of ecology and evolution, and carries potentially important implications for conservation biology. Yet ...not only does this question remain unresolved, it has largely fallen into disregard. With the rapid decrease in sequencing costs, we argue that it is time to revive it.
Surveys of molecular variation in Drosophila melanogaster and Drosophila simulans have suggested that diversity outside of Africa is a subset of that within Africa. It has been argued that reduced ...levels of diversity in non-African populations reflect a population bottleneck, adaptation to temperate climates, or both. Here, I summarize the available single-nucleotide polymorphism data for both species. A simple "out of Africa" bottleneck scenario is consistent with geographic patterns for loci on the X chromosome but not with loci on the autosomes. Interestingly, there is a trend toward lower nucleotide diversity on the X chromosome relative to autosomes in non-African populations of D. melanogaster, but the opposite trend is seen in African populations. In African populations, autosomal inversion polymorphisms in D. melanogaster may contribute to reduced autosome diversity relative to the X chromosome. To elucidate the role that selection might play in shaping patterns of variability, I present a summary of within- and between-species patterns of synonymous and replacement variation in both species. Overall, D. melanogaster autosomes harbor an excess of amino acid replacement polymorphisms relative to D. simulans. Interestingly, range expansion from Africa appears to have had little effect on synonymous-to-replacement polymorphism ratios.
In an elaborate form of inter-species exploitation, many insects hijack plant development to induce novel plant organs called galls that provide the insect with a source of nutrition and a temporary ...home. Galls result from dramatic reprogramming of plant cell biology driven by insect molecules, but the roles of specific insect molecules in gall development have not yet been determined. Here, we study the aphid Hormaphis cornu, which makes distinctive “cone” galls on leaves of witch hazel Hamamelis virginiana. We found that derived genetic variants in the aphid gene determinant of gall color (dgc) are associated with strong downregulation of dgc transcription in aphid salivary glands, upregulation in galls of seven genes involved in anthocyanin synthesis, and deposition of two red anthocyanins in galls. We hypothesize that aphids inject DGC protein into galls and that this results in differential expression of a small number of plant genes. dgc is a member of a large, diverse family of novel predicted secreted proteins characterized by a pair of widely spaced cysteine-tyrosine-cysteine (CYC) residues, which we named BICYCLE proteins. bicycle genes are most strongly expressed in the salivary glands specifically of galling aphid generations, suggesting that they may regulate many aspects of gall development. bicycle genes have experienced unusually frequent diversifying selection, consistent with their potential role controlling gall development in a molecular arms race between aphids and their host plants.
•Novel aphid bicycle genes contribute to plant gall development•Variation in a bicycle gene alters plant gene expression and a gall phenotype•bicycle genes encode a large family of diverse, secreted, cysteine-rich proteins•Many bicycle genes have experienced repeated diversifying selection
Korgaonkar et al. report on novel secreted aphid proteins encoded by bicycle genes. Variation in the bicycle gene determinant of gall color alters expression of targeted plant genes, suggesting that BICYCLE proteins modulate gall development.
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.
Mechanisms of sex chromosome dosage compensation (SCDC) differ strikingly among animals. In Drosophila flies, chromosome-wide transcription is doubled from the single X chromosome in hemizygous (XY) ...males, whereas in Caenorhabditis nematodes, expression is halved for both X copies in homozygous (XX) females 1, 2. Unlike other female-heterogametic (WZ female and ZZ male) animals, moths and butterflies exhibit sex chromosome dosage compensation patterns typically seen only in male-heterogametic species 3. The monarch butterfly carries a newly derived Z chromosome segment that arose from an autosomal fusion with the ancestral Z 4. Using a highly contiguous genome assembly, we show that gene expression is balanced between sexes along the entire Z chromosome but with distinct modes of compensation on the two segments. On the ancestral Z segment, depletion of H4K16ac corresponds to nearly halving of biallelic transcription in males, a pattern convergent to nematodes. Conversely, the newly derived Z segment shows a Drosophila-like mode of compensation, with enriched H4K16ac levels corresponding to doubled monoallelic transcription in females. Our work reveals that, contrary to the expectation of co-opting regulatory mechanisms readily in place, the evolution of plural modes of dosage compensation is also possible along a single sex chromosome within a species.
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•A new chromosome-level assembly is generated for the monarch butterfly•The neo-Z expression is upregulated by 2-fold in females (WZ)•The ancestral-Z expression is downregulated by nearly 2-fold in males (ZZ)•H4K16ac is enriched on neo-Z in females but depleted on ancestral-Z in males
Gu et al. use genomic, transcriptomic, and epigenomic tools to analyze sex chromosome dosage compensation in the monarch butterfly, which carries a neo Z chromosome. They find that the newly derived neo-Z and ancestral Z segments have evolved distinct modes of dosage compensation that mirror Drosophila flies and nematodes, respectively.
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