ABSTRACT
In organisms with the XY sex-determination system, there is an imbalance in the inheritance and transmission of the X chromosome between males and females. Unlike an autosomal allele, an X-linked recessive allele in a female will have phenotypic effects on its male counterpart. Thus, genes located on the X chromosome are of particular interest to researchers in molecular evolution and genetics. Here we present a model for selection with two alleles of X-linkage to understand fitness components associated with genes on the X chromosome. We apply this model to the fitness analysis of an X-linked gene, OdsH (16D), in the fruit fly Drosophila melanogaster. The function of OdsH is involved in sperm production and the gene is rapidly evolving under positive selection. Using site-directed gene targeting, we generated functional and defective OdsH variants tagged with the eye-color marker gene white. We compare the allele frequency changes of the two OdsH variants, each directly competing against a wild-type OdsH allele in concurrent but separate experimental populations. After twenty generations, the two genetically modified OdsH variants displayed a 40% difference in allele frequencies, with the functional OdsH variant demonstrating an advantage over the defective variant. Using maximum likelihood estimation (MLE), we determined the fitness components associated with the OdsH alleles in males and females. Our analysis revealed functional aspects of the fitness determinants associated with OdsH, and that sex-specific fertility and viability consequences both contribute to selection on an X-linked gene.
ABSTRACT
High-sugar diets (HSDs) often lead to obesity and type 2 diabetes, both metabolic syndromes associated with stem cell dysfunction. However, it is unclear whether excess dietary sugar affects stem cells. Here, we report that HSD impairs stem cell function in the intestine and ovaries of female Drosophila prior to the onset of insulin resistance, a hallmark of type 2 diabetes. Although 1â week of HSD leads to obesity, impaired oogenesis and altered lipid metabolism, insulin resistance does not occur. HSD increases glucose uptake by germline stem cells (GSCs) and triggers reactive oxygen species-induced JNK signaling, which reduces GSC proliferation. Removal of excess sugar from the diet reverses these HSD-induced phenomena. A similar phenomenon is found in intestinal stem cells (ISCs), except that HSD disrupts ISC maintenance and differentiation. Interestingly, tumor-like GSCs and ISCs are less responsive to HSD, which may be because of their dependence on glycolytic metabolism and high energy demand, respectively. This study suggests that excess dietary sugar induces oxidative stress and damages stem cells before insulin resistance develops, a mechanism that may also occur in higher organisms.
Subject(s)
Adult Stem Cells , Diabetes Mellitus, Type 2 , Drosophila Proteins , Insulin Resistance , Animals , Female , Drosophila/metabolism , Drosophila Proteins/metabolism , Reactive Oxygen Species/metabolism , Dietary Sugars/metabolism , Adult Stem Cells/metabolism , Neoplastic Stem Cells/metabolism , ObesityABSTRACT
Domestication is the long and complex process underlying the evolution of crops, in which artificial directional selection transformed wild progenitors into the desired form, affecting genomic variation and leaving traces of selection at targeted loci. However, whether genes controlling important domestication traits follow the same evolutionary pattern expected under the standard selective sweep model remains unclear. With whole-genome resequencing of mungbean (Vigna radiata), we investigated this issue by resolving its global demographic history and targeted dissection of the molecular footprints of genes underlying 2 key traits representing different stages of domestication. Mungbean originated in Asia, and the Southeast Asian wild population migrated to Australia about 50 thousand generations ago. Later in Asia, the cultivated form diverged from the wild progenitor. We identified the gene associated with the pod shattering resistance trait, VrMYB26a, with lower expression across cultivars and reduced polymorphism in the promoter region, reflecting a hard selective sweep. On the other hand, the stem determinacy trait was associated with VrDet1. We found that 2 ancient haplotypes of this gene have lower gene expression and exhibited intermediate frequencies in cultivars, consistent with selection favoring independent haplotypes in a soft selective sweep. In mungbean, contrasting signatures of selection were identified from the detailed dissection of 2 important domestication traits. The results suggest complex genetic architecture underlying the seemingly simple process of directional artificial selection and highlight the limitations of genome-scan methods relying on hard selective sweeps.
Subject(s)
Fabaceae , Vigna , Vigna/genetics , Quantitative Trait Loci , Domestication , Fabaceae/genetics , Demography , Selection, GeneticABSTRACT
While the domestication process has been investigated in many crops, the detailed route of cultivation range expansion and factors governing this process received relatively little attention. Here, using mungbean (Vigna radiata var. radiata) as a test case, we investigated the genomes of more than 1000 accessions to illustrate climatic adaptation's role in dictating the unique routes of cultivation range expansion. Despite the geographical proximity between South and Central Asia, genetic evidence suggests mungbean cultivation first spread from South Asia to Southeast, East and finally reached Central Asia. Combining evidence from demographic inference, climatic niche modeling, plant morphology, and records from ancient Chinese sources, we showed that the specific route was shaped by the unique combinations of climatic constraints and farmer practices across Asia, which imposed divergent selection favoring higher yield in the south but short-season and more drought-tolerant accessions in the north. Our results suggest that mungbean did not radiate from the domestication center as expected purely under human activity, but instead, the spread of mungbean cultivation is highly constrained by climatic adaptation, echoing the idea that human commensals are more difficult to spread through the south-north axis of continents.
Mungbean, also known as green gram, is an important crop plant in China, India, the Philippines and many other countries across Asia. Archaeological evidence suggests that humans first cultivated mungbeans from wild relatives in India over 4,000 years ago. However, it remains unclear how cultivation has spread to other countries and whether human activity alone dictated the route of the cultivated mungbean's expansion across Asia, or whether environmental factors, such as climate, also had an impact. To understand how a species of plant has evolved, researchers may collect specimens from the wild or from cultivated areas. Each group of plants of the same species they collect in a given location at a single point in time is known collectively as an accession. Ong et al. used a combination of genome sequencing, computational modelling and plant biology approaches to study more than 1,000 accessions of cultivated mungbean and trace the route of the crop's expansion across Asia. The data support the archaeological evidence that mungbean cultivation first spread from South Asia to Southeast Asia, then spread northwards to East Asia and afterwards to Central Asia. Computational modelling of local climates and the physical characteristics of different mungbean accessions suggest that the availability of water in the local area likely influenced the route. Specifically, accessions from arid Central Asia were better adapted to drought conditions than accessions from wetter South Asia. However, these drought adaptations decreased the yield of the plants, which may explain why the more drought tolerant accessions have not been widely grown in wetter parts of Asia. This study shows that human activity has not solely dictated where mungbean has been cultivated. Instead, both human activity and the various adaptations accessions evolved in response to their local environments shaped the route the crop took across Asia. In the future these findings may help plant breeders to identify varieties of mungbean and other crops with drought tolerance and other potentially useful traits for agriculture.
Subject(s)
Fabaceae , Vigna , Humans , Vigna/genetics , Fabaceae/genetics , Asia , Domestication , Asia, SouthernABSTRACT
Gut bacteria play vital roles in the dietary detoxification, digestion, and nutrient supplementation of hosts during dietary specialization. The roles of gut bacteria in the host can be unveiled by comparing communities of specialist and generalist bacterial species. However, these species usually have a long evolutionary history, making it difficult to determine whether bacterial community differentiation is due to host dietary adaptation or phylogenetic divergence. In this regard, we investigated the bacterial communities from two Araceae-feeding Colocasiomyia species and further performed a meta-analysis by incorporating the published data from Drosophila bacterial community studies. The compositional and functional differentiation of bacterial communities was uncovered by comparing three (Araceae-feeding, mycophagous, and cactophilic) specialists with generalist flies. The compositional differentiation showed that Bacteroidetes and Firmicutes inhabited specialists, while more Proteobacteria lived in generalists. The functional prediction based on the bacterial community compositions suggested that amino acid metabolism and energy metabolism are overrepresented pathways in specialists and generalists, respectively. The differences were mainly associated with the higher utilization of structural complex carbohydrates, protein utilization, vitamin B12 acquisition, and demand for detoxification in specialists than in generalists. The complementary roles of bacteria reveal a connection between gut bacterial communities and fly dietary specialization. IMPORTANCE Gut bacteria may play roles in the dietary utilization of hosts, especially in specialist animals, during long-term host-microbe interaction. By comparing the gut bacterial communities between specialist and generalist drosophilid flies, we found that specialists harbor more bacteria linked to complex carbohydrate degradation, amino acid metabolism, vitamin B12 formation, and detoxification than do generalists. This study reveals the roles of gut bacteria in drosophilid species in dietary utilization.
Subject(s)
Diptera , Gastrointestinal Microbiome , Amino Acids , Animals , Bacteria/genetics , Phylogeny , RNA, Ribosomal, 16S , VitaminsABSTRACT
BACKGROUND: Phenology data collected recently for about 300 accessions of Vigna radiata (mungbean) is an invaluable resource for investigation of impacts of climatic factors on plant development. RESULTS: We developed a new mathematical model that describes the dynamic control of time to flowering by daily values of maximal and minimal temperature, precipitation, day length and solar radiation. We obtained model parameters by adaptation to the available experimental data. The models were validated by cross-validation and used to demonstrate that the phenology of adaptive traits, like flowering time, is strongly predicted not only by local environmental factors but also by plant geographic origin and genotype. CONCLUSIONS: Of local environmental factors maximal temperature appeared to be the most critical factor determining how faithfully the model describes the data. The models were applied to forecast time to flowering of accessions grown in Taiwan in future years 2020-2030.
Subject(s)
Climate , Flowers/growth & development , Models, Biological , Vigna/growth & development , Adaptation, Physiological , Genotype , Time Factors , Vigna/geneticsABSTRACT
BACKGROUND: Mungbean (Vigna radiata (L.) R. Wilczek, or green gram) is important tropical and sub-tropical legume and a rich source of dietary protein and micronutrients. In this study we employ GWAS to examine the genetic basis of variation in several important traits in mungbean, using the mini-core collection established by the World Vegetable Center, which includes 296 accessions that represent the major market classes. This collection has been grown in a common field plot in southern European part of Russia in 2018. RESULTS: We used 5041 SNPs in 293 accessions that passed strict filtering for genetic diversity, linkage disequilibrium, population structure and GWAS analysis. Polymorphisms were distributed among all chromosomes, but with variable density. Linkage disequilibrium decayed in approximately 105 kb. Four distinct subgroups were identified within 293 accessions with 70% of accessions attributed to one of the four populations. By performing GWAS on the mini-core collection we have found several loci significantly associated with two important agronomical traits. Four SNPs associated with possibility of maturation in Kuban territory of Southern Russia in 2018 were identified within a region of strong linkage which contains genes encoding zinc finger A20 and an AN1 domain stress-associated protein. CONCLUSIONS: The core collection of mungbean established by the World Vegetable Center is a valuable resource for mungbean breeding. The collection has been grown in southern European part of Russia in 2018 under incidental stresses caused by abnormally hot weather and different photoperiod. We have found several loci significantly associated with color of hypocotyl and possibility of maturation under these stressful conditions. SNPs associated with possibility of maturation localize to a region on chromosome 2 with strong linkage, in which genes encoding zinc finger A20 and AN1 domain stress associated protein (SAP) are located. Phenotyping of WorldVeg collection for maturation traits in temperate climatic locations is important as phenology remains a critical breeding target for mungbean. As demand rises for mungbean, production in temperate regions with shorter growing seasons becomes crucial to keep up with needs. Uncovering SNPs for phenology traits will speed breeding efforts.
Subject(s)
Biological Specimen Banks , Polymorphism, Single Nucleotide , Vigna/genetics , Genome-Wide Association Study , Linkage DisequilibriumABSTRACT
Segmental duplications are an important class of mutations. Because a large proportion of segmental duplications may often be strongly deleterious, high frequency or fixed segmental duplications may represent only a tiny fraction of the mutational input. To understand the emergence and elimination of segmental duplications, we survey polymorphic duplications, including tandem and interspersed duplications, in natural populations of Drosophila by haploid embryo genomes. As haploid embryos are not expected to be heterozygous, the genome, sites of heterozygosity (referred to as pseudoheterozygous sites [PHS]), may likely represent recent duplications that have acquired new mutations. Among the 29 genomes of Drosophila melanogaster, we identify 2,282 polymorphic PHS duplications (linked PHS regions) in total or 154 PHS duplications per genome. Most PHS duplications are small (83.4% < 500 bp), Drosophila melanogaster lineage specific, and strain specific (72.6% singletons). The excess of the observed singleton PHS duplications deviates significantly from the neutral expectation, suggesting that most PHS duplications are strongly deleterious. In addition, these small segmental duplications are not evenly distributed in genomic regions and less common in noncoding functional element regions. The underrepresentation in RNA polymerase II binding sites and regions with active histone modifications is correlated with ages of duplications. In conclusion, small segmental duplications occur frequently in Drosophila but rapidly eliminated by natural selection.
Subject(s)
Drosophila melanogaster/genetics , Gene Duplication , Animals , Genome, Insect , Selection, GeneticABSTRACT
BACKGROUND: Long non-coding RNAs (lncRNAs) are important in various biological processes, but very few studies on lncRNA have been conducted in birds. To identify IncRNAs expressed during feather development, we analyzed single-stranded RNA-seq (ssRNA-seq) data from the anterior and posterior dorsal regions during zebra finch (Taeniopygia guttata) embryonic development. Using published transcriptomic data, we further analyzed the evolutionary conservation of IncRNAs in birds and amniotes. RESULTS: A total of 1,081 lncRNAs, including 965 intergenic lncRNAs (lincRNAs), 59 intronic lncRNAs, and 57 antisense lncRNAs (lncNATs), were identified using our newly developed pipeline. These avian IncRNAs share similar characteristics with lncRNAs in mammals, such as shorter transcript length, lower exon number, lower average expression level and less sequence conservation than mRNAs. However, the proportion of lncRNAs overlapping with transposable elements in birds is much lower than that in mammals. We predicted the functions of IncRNAs based on the enriched functions of co-expressed protein-coding genes. Clusters of lncRNAs associated with natal down development were identified. The sequences and expression levels of candidate lncRNAs that shared conserved sequences among birds were validated by qPCR in both zebra finch and chicken. Finally, we identified three highly conserved lncRNAs that may be associated with natal down development. CONCLUSIONS: Our study provides the first systematical identification of avian lncRNAs using ssRNA-seq analysis and offers a resource of embryonically expressed lncRNAs in zebra finch. We also predicted the biological function of identified lncRNAs.
Subject(s)
Evolution, Molecular , Finches/genetics , RNA, Long Noncoding/genetics , Transcriptome , Animals , Cluster Analysis , Computational Biology/methods , Gene Expression Profiling , Genomics/methodsABSTRACT
Birds can be classified into altricial and precocial. The hatchlings of altricial birds are almost naked, whereas those of precocial birds are covered with natal down. This regulatory divergence is thought to reflect environmental adaptation, but the molecular basis of the divergence is unclear. To address this issue, we chose the altricial zebra finch and the precocial chicken as the model animals. We noted that zebra finch hatchlings show natal down growth suppressed anterior dorsal (AD) skin but partially down-covered posterior dorsal (PD) skin. Comparing the transcriptomes of AD and PD skins, we found that the feather growth promoter SHH (sonic hedgehog) was expressed higher in PD skin than in AD skin. Moreover, the data suggested that the FGF (fibroblast growth factor)/Mitogen-activated protein kinase (MAPK) signaling pathway is involved in natal down growth suppression and that FGF16 is a candidate upstream signaling suppressor. Ectopic expression of FGF16 on chicken leg skin showed downregulation of SHH, upregulation of the feather growth suppressor FGF10, and suppression of feather bud elongation, similar to the phenotype found in zebra finch embryonic AD skin. Therefore, we propose that FGF16-related signals suppress natal down elongation and cause the naked AD skin in zebra finch. Our study provides insights into the regulatory divergence in natal down formation between precocial and altricial birds.
Subject(s)
Chickens/growth & development , Feathers/growth & development , Finches/growth & development , Animals , Biological Evolution , Chickens/metabolism , Evolution, Molecular , Feathers/metabolism , Fibroblast Growth Factors/genetics , Fibroblast Growth Factors/metabolism , Finches/metabolism , Gene Expression Regulation , Hedgehog Proteins/metabolism , Mitogen-Activated Protein Kinases/metabolismABSTRACT
Widespread premature termination codon mutations (PTCs) were recently observed in human and fly populations. We took advantage of the population resequencing data in the Drosophila Genetic Reference Panel to investigate how the expression profile and the evolutionary age of genes shaped the allele frequency distribution of PTCs. After generating a high-quality data set of PTCs, we clustered genes harboring PTCs into three categories: genes encoding low-frequency PTCs (≤ 1.5%), moderate-frequency PTCs (1.5-10%), and high-frequency PTCs (>10%). All three groups show narrow transcription compared with PTC-free genes, with the moderate- and high-PTC frequency groups showing a pronounced pattern. Moreover, nearly half (42%) of the PTC-encoding genes are not expressed in any tissue. Interestingly, the moderate-frequency PTC group is strongly enriched for genes expressed in midgut, whereas genes harboring high-frequency PTCs tend to have sex-specific expression. We further find that although young genes born in the last 60 My compose a mere 9% of the genome, they represent 16%, 30%, and 50% of the genes containing low-, moderate-, and high-frequency PTCs, respectively. Among DNA-based and RNA-based duplicated genes, the child copy is approximately twice as likely to contain PTCs as the parent copy, whereas young de novo genes are as likely to encode PTCs as DNA-based duplicated new genes. Based on these results, we conclude that expression profile and gene age jointly shaped the landscape of PTC-mediated gene loss. Therefore, we propose that new genes may need a long time to become stably maintained after the origination.
Subject(s)
Codon, Nonsense , Computational Biology/methods , Drosophila Proteins/genetics , Drosophila melanogaster/genetics , Animals , Chromosomes , Evolution, Molecular , Gene Expression Profiling , Sequence Analysis, DNA , Tissue DistributionABSTRACT
Parthenogenesis has evolved independently in more than 10 Drosophila species. Most cases are tychoparthenogenesis, which is occasional or accidental parthenogenesis in normally bisexual species with a low hatching rate of eggs produced by virgin females; this form is presumed to be an early stage of parthenogenesis. To address how parthenogenesis and sexual reproduction coexist in Drosophila populations, we investigated several reproductive traits, including the fertility, parthenogenetic capability, diploidization mechanisms, and mating propensity of parthenogenetic D. albomicans. The fertility of mated parthenogenetic females was significantly higher than that of virgin females. The mated females could still produce parthenogenetic offspring but predominantly produced offspring by sexual reproduction. Both mated parthenogenetic females and their parthenogenetic-sexual descendants were capable of parthenogenesis. The alleles responsible for parthenogenesis can be propagated through both parthenogenesis and sexual reproduction. As diploidy is restored predominantly by gamete duplication, heterozygosity would be very low in parthenogenetic individuals. Hence, genetic variation in parthenogenetic genomes would result from sexual reproduction. The mating propensity of females after more than 20 years of isolation from males was decreased. If mutations reducing mating propensities could occur under male-limited conditions in natural populations, decreased mating propensity might accelerate tychoparthenogenesis through a positive feedback mechanism. This process provides an opportunity for the evolution of obligate parthenogenesis. Therefore, the persistence of facultative parthenogenesis may be an adaptive reproductive strategy in Drosophila when a few founders colonize a new niche or when small populations are distributed at the edge of a species' range, consistent with models of geographical parthenogenesis.
Subject(s)
Drosophila/genetics , Genetic Variation , Parthenogenesis/genetics , Sexual Behavior, Animal , Animals , Diploidy , Drosophila/physiology , Evolution, Molecular , Female , Fertility/genetics , Genetic Fitness , Genotype , Male , Phenotype , Reproduction/genetics , Species SpecificityABSTRACT
Many insects feed on only one or a few types of host. These host specialists often evolve a preference for chemical cues emanating from their host and develop mechanisms for circumventing their host's defenses. Adaptations like these are central to evolutionary biology, yet our understanding of their genetics remains incomplete. Drosophila sechellia, an emerging model for the genetics of host specialization, is an island endemic that has adapted to chemical toxins present in the fruit of its host plant, Morinda citrifolia. Its sibling species, D. simulans, and many other Drosophila species do not tolerate these toxins and avoid the fruit. Earlier work found a region with a strong effect on tolerance to the major toxin, octanoic acid, on chromosome arm 3R. Using a novel assay, we narrowed this region to a small span near the centromere containing 18 genes, including three odorant binding proteins. It has been hypothesized that the evolution of host specialization is facilitated by genetic linkage between alleles contributing to host preference and alleles contributing to host usage, such as tolerance to secondary compounds. We tested this hypothesis by measuring the effect of this tolerance locus on host preference behavior. Our data were inconsistent with the linkage hypothesis, as flies bearing this tolerance region showed no increase in preference for media containing M. citrifolia toxins, which D. sechellia prefers. Thus, in contrast to some models for host preference, preference and tolerance are not tightly linked at this locus nor is increased tolerance per se sufficient to change preference. Our data are consistent with the previously proposed model that the evolution of D. sechellia as a M. citrifolia specialist occurred through a stepwise loss of aversion and gain of tolerance to M. citrifolia's toxins.
Subject(s)
Drosophila/genetics , Drosophila/physiology , Adaptation, Physiological/genetics , Animals , Caprylates/toxicity , Chromosome Mapping , Evolution, Molecular , Female , Food Preferences , Genes, Insect , Male , Models, Genetic , Morinda/chemistry , Morinda/toxicity , Receptors, Odorant/genetics , Species Specificity , Toxins, Biological/chemistryABSTRACT
Odysseus (OdsH) has been identified as a hybrid male sterility gene between Drosophila mauritiana and D. simulans with accelerated evolutionary rate in both expression and DNA sequence. Loss of a testis-specific expression of OdsH causes male fertility defect in D. melanogaster. Yet, the underlying mechanisms at the cellular level are unknown. In an attempt to identify the possible mechanisms and functional roles of OdsH in spermatogenesis, the cell numbers at different developmental stages during spermatogenesis between the OdsH null mutant and wild-type flies were compared. The results showed that the early developing germ cells, including spermatogonia and spermatocytes, were reduced in the OdsH mutant males. In addition, the number of germline stem cells in aged males was also reduced, presumably due to the disruption of germline stem cell maintenance, which resulted in more severe fertility defect. These results suggest that the function of the enhancement of sperm production by OdsH acted across males of all ages.
Subject(s)
Drosophila Proteins/genetics , Drosophila melanogaster/genetics , Homeodomain Proteins/genetics , Mutation , Animals , Drosophila melanogaster/growth & development , Drosophila melanogaster/physiology , Fertility/genetics , Infertility, Male/genetics , Male , Spermatocytes/growth & development , Spermatogenesis/genetics , Spermatogonia/growth & developmentABSTRACT
The relative importance of mutation, selection, and biased gene conversion to patterns of base composition variation in Drosophila melanogaster, and to a lesser extent, D. simulans, has been investigated for many years. However, genomic data from sufficiently large samples to thoroughly characterize patterns of base composition polymorphism within species have been lacking. Here, we report a genome-wide analysis of coding and noncoding polymorphism in a large sample of inbred D. melanogaster strains from Raleigh, North Carolina. Consistent with previous results, we observed that AT mutations fix more frequently than GC mutations in D. melanogaster. Contrary to predictions of previous models of codon usage in D. melanogaster, we found that synonymous sites segregating for derived AT polymorphisms were less skewed toward low frequencies compared with sites segregating a derived GC polymorphism. However, no such pattern was observed for comparable base composition polymorphisms in noncoding DNA. These results suggest that AT-ending codons could currently be favored by natural selection in the D. melanogaster lineage.
Subject(s)
Drosophila melanogaster/genetics , Evolution, Molecular , Genome, Insect , Animals , Base Composition , Mutation , Open Reading Frames , Polymorphism, Single Nucleotide , Population/genetics , Untranslated RegionsABSTRACT
Postmating reproductive isolation is often manifested as hybrid male sterility, for which X-linked genes are overrepresented (the so-called large X effect). In contrast, X-linked genes are significantly under-represented among testis-expressing genes. This seeming contradiction may be germane to the X:autosome imbalance hypothesis on hybrid sterility, in which the X-linked effect is mediated mainly through the misexpression of autosomal genes. In this study, we compared gene expression in fertile and sterile males in the hybrids between two Drosophila species. These hybrid males differ only in a small region of the X chromosome containing the Ods-site homeobox (OdsH) (also known as Odysseus) locus of hybrid sterility. Of genes expressed in the testis, autosomal genes were, indeed, more likely to be misexpressed than X-linked genes under the sterilizing action of OdsH. Since this mechanism of X:autosome interaction is only associated with spermatogenesis, a connection between X:autosome imbalance and the high rate of hybrid male sterility seems plausible.
Subject(s)
Genes, X-Linked , Infertility, Male/genetics , Spermatogenesis/genetics , Testis/metabolism , Animals , Chimera/genetics , Drosophila/genetics , Drosophila Proteins/metabolism , Fertility/genetics , Gene Expression/genetics , Genetic Loci , Genome-Wide Association Study , Homeodomain Proteins/metabolism , MaleABSTRACT
Frequent gene duplications in the genome incessantly supply new genetic materials for functional innovation presumably driven by positive Darwinian selection. This mechanism in the desaturase gene family has been proposed to be important in triggering the pheromonal diversification in insects. With the recent completion of a dozen Drosophila genomes, a genome-wide perspective is possible. In this study, we first identified homologs of desaturase genes in 12 Drosophila species and noted that while gene duplication events are relatively frequent, gene losses are not scarce, especially in the desat1-desat2-desatF clade. By reconciling the gene tree with species phylogeny and the chromosomal synteny of the sequenced Drosophila genomes, at least one gene loss in desat2 and a minimum of six gene gains (resulting in seven desatF homologs, alpha-eta), three gene losses and one relocation in desatF were inferred. Upon branching off the ancestral desat1 lineage, both desat2 and desatF gained novel functions through accelerating protein evolution. The amino acid residues under positive selection located near the catalytic sites and the C-terminal region might be responsible for altered substrate selectivity between closely related species. The association between the expression pattern of desatF-alpha and the chemical composition of cuticular hydrocarbons implies that the ancestral function of desatF-alpha is the second desaturation at the four carbons after the first double bond in diene synthesis, and the shift from bisexual to female-specific expression in desatF-alpha occurred in the ancestral lineage of Drosophila melanogaster subgroup. A relationship between the number of expressed desatF homologs and the diene diversification has also been observed. These results suggest that the molecular diversification of fatty acid desaturases after recurrent gene duplication plays an important role in pheromonal diversity in Drosophila.
Subject(s)
Drosophila/enzymology , Drosophila/genetics , Evolution, Molecular , Fatty Acid Desaturases/genetics , Gene Duplication , Animals , Drosophila melanogaster/enzymology , Drosophila melanogaster/genetics , PhylogenyABSTRACT
The importance of gene duplication in evolution has long been recognized. Because duplicated genes are prone to diverge in function, gene duplication could plausibly play a role in species differentiation. However, experimental evidence linking gene duplication with speciation is scarce. Here, we show that a hybrid-male sterility gene, Odysseus (OdsH), arose by gene duplication in the Drosophila genome. OdsH has evolved at a very high rate, whereas its most immediate paralog, unc-4, is nearly identical among species in the Drosophila melanogaster subgroup. The disparity in their sequence evolution is echoed by the divergence in their expression patterns in both soma and reproductive tissues. We suggest that duplicated genes that have yet to evolve a stable function at the time of speciation may be candidates for "speciation genes," which is broadly defined as genes that contribute to differential adaptation between species.
Subject(s)
Drosophila Proteins/genetics , Drosophila/genetics , Gene Duplication , Genes, Insect , Homeodomain Proteins/genetics , Amino Acid Sequence , Animals , Drosophila/classification , Drosophila melanogaster/classification , Drosophila melanogaster/genetics , Evolution, Molecular , Female , Gene Expression , Infertility, Male/genetics , Male , Molecular Sequence Data , Sequence Homology, Amino Acid , Species SpecificityABSTRACT
To understand how postmating isolation is connected to the normal process of species divergence and why hybrid male sterility is often the first sign of speciation, we analyzed the Odysseus (OdsH) gene of hybrid male sterility in Drosophila. We carried out expression analysis, transgenic study, and gene knockout. The combined evidence suggests that the sterility phenotype represents a novel manifestation of the gene function rather than the reduction or loss of the normal one. The gene knockout experiment identified the normal function of OdsH as a modest enhancement of sperm production in young males. The implication of a weak effect of OdsH on the normal phenotype but a strong influence on hybrid male sterility is discussed in light of Haldane's rule of postmating isolation.