Descriptions of recently evolved genes suggest several mechanisms of origin including exon shuffling, gene fission͞fusion, retrotransposition, duplication-divergence, and lateral gene transfer, all of which involve recruitment of preexisting genes or genetic elements into new function. The importance of noncoding DNA in the origin of novel genes remains an open question. We used the well annotated genome of the genetic model system Drosophila melanogaster and genome sequences of related species to carry out a whole-genome search for new D. melanogaster genes that are derived from noncoding DNA. Here, we describe five such genes, four of which are X-linked. Our RT-PCR experiments show that all five putative novel genes are expressed predominantly in testes. These data support the idea that these novel genes are derived from ancestral noncoding sequence and that new, favored genes are likely to invade populations under selective pressures relating to male reproduction. adaptation ͉ comparative genomics ͉ lineage-specific ͉ de novo gene U nderstanding the genetic basis of adaptation remains a key priority for evolutionary biologists. Most adaptation likely results from modification of ancestral genetic function. Such modifications include coding sequence substitutions (1) and the origination of novel genes by partial or complete duplication of preexisting genes (2). The contribution of more radical ''de novo'' genetic changes to adaptive divergence, such as the recruitment of noncoding DNA into coding function, remains an open question. Although there are some rare examples that support partial recruitment of noncoding DNA into new genes (3, 4), there is no evidence thus far for novel genes derived primarily from ancestrally noncoding DNA. Such de novo genes would be difficult to identify for two reasons. First, novel gene discovery, which often occurs by serendipitous discovery of lineage-specific exon duplication (5, 6), biases against de novo gene identification. Second, if novel genes evolve rapidly under directional selection and͞or if the associated ancestral noncoding DNA evolves rapidly under low functional constraint, there may be only a brief evolutionary window during which a new gene and its noncoding ancestor can be identified. Results and DiscussionWe took advantage of the recently assembled Drosophila genomes to carry out an analysis of lineage-specific de novo genes using the annotated model system genome of Drosophila melanogaster and the genome sequences of its close relatives. We generated a preliminary list of candidate genes from annotated D. melanogaster genes that returned poor hits in an automated BLASTN analysis against the genomes of Drosophila yakuba, Drosophila erecta, and Drosophila ananassae (see Methods). This search should exclude novel genes that are primarily composed of D. melanogaster-specific duplications of preexisting functional exons present in the common ancestor of all four species. The list of D. melanogaster and͞or Drosophila simulans-specific genes was reduced by retaini...
Drosophila melanogaster shows clinal variation along latitudinal transects on multiple continents for several phenotypes, allozyme variants, sequence variants, and chromosome inversions. Previous investigation suggests that many such clines are due to spatially varying selection rather than demographic history, but the genomic extent of such selection is unknown. To map differentiation throughout the genome, we hybridized DNA from temperate and subtropical populations to Affymetrix tiling arrays. The dense genomic sampling of variants and low level of linkage disequilibrium in D. melanogaster enabled identification of many small, differentiated regions. Many regions are differentiated in parallel in the United States and Australia, strongly supporting the idea that they are influenced by spatially varying selection. Genomic differentiation is distributed nonrandomly with respect to gene function, even in regions differentiated on only one continent, providing further evidence for the role of selection. These data provide candidate genes for phenotypes known to vary clinally and implicate interesting new processes in genotype-by-environment interactions, including chorion proteins, proteins regulating meiotic recombination and segregation, gustatory and olfactory receptors, and proteins affecting synaptic function and behavior. This portrait of differentiation provides a genomic perspective on adaptation and the maintenance of variation through spatially varying selection.T HE amount and genomic distribution of polymorphism may be influenced by genetic drift, by mutation-selection balance, and by various forms of positive selection such as spatially varying selection, heterozygote advantage, or negative frequency-dependent selection. Spatially varying selection can generate allelefrequency differences between populations in spite of gene flow and lead to local adaptation, which is of particular interest as an intermediate step between intra-and interspecies variation (Felsenstein 1976;Endler 1977;Barton 1983).Drosophila melanogaster has been a model system for investigating the forces maintaining polymorphism for many decades. Indeed, differentiation along latitudinal clines in this species is one of the most thoroughly documented cases of spatially varying selection ( and Singh 1991;Berry and Kreitman 1993;Long and Singh 1995;Gockel et al. 2002;Kennington et al. 2003). The observations that clinal variation is strongly associated with easily measurable phenotypes affecting fitness (Eanes 1999;Gockel et al. 2002;Calboli et al. 2003;Norry et al. 2004;Kennington et al. 2007) and that clines for a number of phenotypes and genetic variants appear to have been independently established on multiple continents (De Jong and Bochdanovits 2003) also strongly support the proposition that many clinal variants are under spatially varying selection and that the biology of temperate and tropical populations may be quite different.Nevertheless, these data represent a small and highly biased picture of the phenotypes and...
The genotypic signature of spatially varying selection is ubiquitous across the Drosophila melanogaster genome. Spatially structured adaptive phenotypic differences are also commonly found, particularly along New World and Australian latitudinal gradients. However, investigation of gene expression variation in one or multiple environments across these well-studied populations is surprisingly limited. Here, we report genome-wide transcript levels of tropical and temperate eastern Australian populations reared at two temperatures. As expected, a large number of genes exhibit geographic origin-dependent expression plasticity. Less expected was evidence for an enrichment of down-regulated genes in both temperate and tropical populations when lines were reared at the temperature less commonly encountered in the native range; that is, evidence for significant differences in a "directionality" of plasticity across these two climatic regions. We also report evidence of small scale "neighborhood effects" around those genes significant for geographic origin-dependent plasticity, a result consistent with the evolution of high level, likely chromatin based gene regulation during range expansion in D. melanogaster populations.
Heterochromatin is the gene-poor, satellite-rich eukaryotic genome compartment that supports many essential cellular processes. The functional diversity of proteins that bind and often epigenetically define heterochromatic DNA sequence reflects the diverse functions supported by this enigmatic genome compartment. Moreover, heterogeneous signatures of selection at chromosomal proteins often mirror the heterogeneity of evolutionary forces that act on heterochromatic DNA. To identify new such surrogates for dissecting heterochromatin function and evolution, we conducted a comprehensive phylogenomic analysis of the Heterochromatin Protein 1 gene family across 40 million years of Drosophila evolution. Our study expands this gene family from 5 genes to at least 26 genes, including several uncharacterized genes in Drosophila melanogaster. The 21 newly defined HP1s introduce unprecedented structural diversity, lineage-restriction, and germline-biased expression patterns into the HP1 family. We find little evidence of positive selection at these HP1 genes in both population genetic and molecular evolution analyses. Instead, we find that dynamic evolution occurs via prolific gene gains and losses. Despite this dynamic gene turnover, the number of HP1 genes is relatively constant across species. We propose that karyotype evolution drives at least some HP1 gene turnover. For example, the loss of the male germline-restricted HP1E in the obscura group coincides with one episode of dramatic karyotypic evolution, including the gain of a neo-Y in this lineage. This expanded compendium of ovary- and testis-restricted HP1 genes revealed by our study, together with correlated gain/loss dynamics and chromosome fission/fusion events, will guide functional analyses of novel roles supported by germline chromatin.
In most eukaryotes, telomerase counteracts chromosome erosion by adding repetitive sequence to terminal ends. Drosophila melanogaster instead relies on specialized retrotransposons that insert exclusively at telomeres. This exchange of goods between host and mobile element-wherein the mobile element provides an essential genome service and the host provides a hospitable niche for mobile element propagation-has been called a "genomic symbiosis." However, these telomerespecialized, jockey family retrotransposons may actually evolve to "selfishly" overreplicate in the genomes that they ostensibly serve. Under this model, we expect rapid diversification of telomere-specialized retrotransposon lineages and, possibly, the breakdown of this ostensibly symbiotic relationship. Here we report data consistent with both predictions. Searching the raw reads of the 15-Myr-old melanogaster species group, we generated de novo jockey retrotransposon consensus sequences and used phylogenetic tree-building to delineate four distinct telomere-associated lineages. Recurrent gains, losses, and replacements account for this retrotransposon lineage diversity. In Drosophila biarmipes, telomere-specialized elements have disappeared completely. De novo assembly of long reads and cytogenetics confirmed this species-specific collapse of retrotransposon-dependent telomere elongation. Instead, telomere-restricted satellite DNA and DNA transposon fragments occupy its terminal ends. We infer that D. biarmipes relies instead on a recombination-based mechanism conserved from yeast to flies to humans. Telomeric retrotransposon diversification and disappearance suggest that persistently "selfish" machinery shapes telomere elongation across Drosophila rather than completely domesticated, symbiotic mobile elements.
Dosage compensation refers to the equalization of X-linked gene transcription among heterogametic and homogametic sexes. In Drosophila, the dosage compensation complex (DCC) mediates the twofold hypertranscription of the single male X chromosome. Loss-of-function mutations at any DCC protein-coding gene are male lethal. Here we report a population genetic analysis suggesting that four of the five core DCC proteins-MSL1, MSL2, MSL3, and MOF-are evolving under positive selection in D. melanogaster. Within these four proteins, several domains that range in function from X chromosome localization to proteinprotein interactions have elevated, D. melanogaster-specific, amino acid divergence.
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