Drosophila chemoreceptor gene evolution: selection, specialization and genome size

Chemoperception plays a key role in adaptation and speciation in animals, and the senses of olfaction and gustation are mediated by gene families which show large variation in repertoire size among species. In Drosophila, there are around 60 loci of each type and it is thought that ecological specialization influences repertoire size, with increased pseudogenization of loci. Here, we analyse the size of the gustatory and olfactory repertoires among the genomes of 12 species of Drosophila . We find that repertoire size varies substantially and the loci are evolving by duplication and pseudogenization, with striking examples of lineage-specific duplication. Selection analyses imply that the majority of loci are subject to purifying selection, but this is less strong in gustatory loci and in loci prone to duplication. In contrast to some other studies, we find that few loci show statistically significant evidence of positive selection. Overall genome size is strongly correlated with the proportion of duplicated chemoreceptor loci, but genome size, specialization and endemism may be interrelated in their influence on repertoire size.     

Quantitative genetic variation and selection of enzyme activities in Drosophila melanogaster

The nature of the genetic variation for the activity of three enzymes (α-GPD, ME, and SOD) was studied by means of analyses of variance among full-sib and half-sib families. The results presented here indicate that the genetic variation of activity of these enzymes consist primarily of non-additive genetic variance. A moderate level of additive genetic variation was found only for α-GPD activity. We also examined the question whether an association exists between enzyme activities and selection for preadult developmental time. Using the method developed by Lande and Arnold (1983), significant directional selection was observed for α-GPD activity.     

A novel gene family NBPF: intricate structure generated by gene duplications during primate evolution

Partial and complete genome duplications occurred during evolution and resulted in the creation of new genes and gene families. We identified a novel and intricate human gene family located primarily in regions of segmental duplications on human chromosome 1. We named it NBPF, for neuroblastoma breakpoint family, because one of its members is disrupted by a chromosomal translocation in a neuroblastoma patient. The NBPF genes have a repetitive structure with high intragenic and intergenic sequence similarity in both coding and noncoding regions. These similarities might expose these genomic regions to illegitimate recombination, resulting in structural variation in the NBPF genes. The encoded proteins contain a highly conserved domain of unknown function, which we have named the NBPF repeat. In silico analysis combined with the isolation of multiple full-length cDNA clones showed that several members of this gene family are abundantly expressed in a large variety of tissues and cell lines. Strikingly, no discernable orthologues could be identified in the completed genomes of fruit fly, nematode, mouse, or rat, but sequences with low homology could be isolated from the draft canine and bovine genomes. Interestingly, this gene family shows primate-specific duplications that result in species-specific arrays of NBPF homologous sequences. Overall, this novel NBPF family reflects the continuous evolution of primate genomes that resulted in large physiological differences, and its potential role in this process is discussed.     

Characterization of HSCD5, a novel human stearoyl-CoA desaturase unique to primates

Stearoyl-CoA desaturase (SCD) is an integral membrane protein of the endoplasmic reticulum (ER) that catalyzes the formation of monounsaturated fatty acids from saturated fatty acids. Recent studies suggest that SCD is a key regulator of energy metabolism and has implications in dislipidemia and obesity. Four SCD isoforms (SCD1-4) have been identified in mouse. In human, only one SCD isoform has been characterized so far. Here we report that the previously reported human ACOD4 gene encodes a distinct stearoyl-CoA desaturase, hSCD5. GenBank database mining revealed orthologues of hSCD5 in the primates, but not in the rodents. In transiently transfected 293 cells, hSCD5 co-localized with calnexin on ER membrane. Microsome fractions prepared from hSCD1 and hSCD5 transfected cells displayed similar delta 9 desaturase activity. Quantitative real-time RT-PCR analysis suggested that hSCD5 was abundantly expressed in adult brain and pancreas. These data suggested that hSCD5 plays a role distinct from that of hSCD1 during development and in normal physiological conditions.     

Population genetics and geographic variation of alcohol dehydrogenase (Adh) paralogs and glucose-6-phosphate dehydrogenase (G6pd) in Drosophila mojavensis

Populations of Drosophila mojavensis from the deserts of the Baja California peninsula and mainland Mexico utilize different cactus hosts with different alcohol contents. The enzyme alcohol dehydrogenase (ADH) has been proposed to play an important role in the adaptation of Drosophila species to their environment. This study investigates the role of ADH in the adaptation of the cactophilic D. mojavensis to its cactus host. In D. mojavensis and its sibling species, D. arizonae, the Adh gene has duplicated, giving rise to a larval/ovarian form (Adh-1) and an adult form (Adh-2). Studies of sequence variation presented here indicate that the Adh paralogs have followed different evolutionary trajectories. Adh-1 exhibits an excess of fixed amino acid replacements, suggesting adaptive evolution, which could have been a result of several host shifts that occurred during the divergence of D. mojavensis. A 17-bp intron haplotype polymorphism segregates in Adh-2 and has markedly different frequencies in the Baja and mainland populations. The presence of the intron polymorphism suggests possible selection for the maintenance of pre-mRNA structure. Finally, this study supports the proposed Baja California origination of D. mojavensis and subsequent colonization of the mainland accompanied by a host shift.     

Spatial variation of biochemical and ecological phenotypes in Drosophila: Electrophoretic and quantitative variation

Electrophoretic variation at three enzyme loci-alcohol dehydrogenase (Adh), glycerophosphate dehydrogenase (Gpdh), triosephosphate isomerase (Tpi)- is compared in Australian Drosophila melanogaster populations at three levels of spatial heterogeneity; among breeding sites, within populations, and between populations at the geographic level. Heterogeneity at the breeding site level greatly exceeds that among adults within populations, indicating greater intermixing at the mobile adult stage than at the developmentally immature and less migratory larval stage. Heterogeneity at the microspatial level is large relative to the geographic level at two of these loci. Spatial patterns of variation in ecological phenotypes are also considered. It is argued that electrophoretic variants may contribute little to an understanding of this quantitative variation, and that a more useful approach in ecological genetics is to consider ecological phenotypes as primary data.     

Molecular evolution and population genetics of duplicated accessory gland protein genes in Drosophila

To investigate the potential importance of gene duplication in D. melanogaster accessory gland protein (Acp) gene evolution we carried out a computational analysis comparing annotated D. melanogaster Acp genes to the entire D. melanogaster genome. We found that two known Acp genes are actually members of small multigene families. Polymorphism and divergence data from these duplicated genes suggest that in at least four cases, protein divergence between D. melanogaster and D. simulans is a result of directional selection. One putative Acp revealed by our computational analysis shows evidence of a recent selective sweep in a non-African population (but not in an African population). These data support the idea that selection on reproduction-related genes may drive divergence of populations within species, and strengthen the conclusion that Acps may often be under directional selection in Drosophila.     

Gene expression and morphogenesis during the deposition of Drosophila wing cuticle

The exoskeleton of insects and other arthropods is a very versatile material that is characterized by a complex multilayer structure. In Sobala and Adler (2016) we analyzed the process of wing cuticle deposition by RNAseq and electron microscopy. In this extra view we discuss the unique aspects of the envelope the first and most outermost layer and the gene expression program seen at the end of cuticle deposition. We discussed the role of undulae in the deposition of cuticle and how the hydrophobicity of wing cuticle arises.     

The relationship between gene dosage,gene expression,and sex in Drosophila

In Drosophila, the ratio of the number of X chromosomes to sets of other chromosomes initiates a series of events which result in sexual differentiation. In addition, this ratio establishes dosage compensation, a mechanism which equalizes the products of X-linked genes in males and females. The present review discusses possible genetic entities responsible for the interpretation of chromosomal sex and subsequent sex-mediated regulation during development.     

Dramatic expansion and developmental expression diversification of the methuselah gene family during recent Drosophila evolution

Functional studies of the methuselah/methuselah-like (mth/mthl) gene family have focused on the founding member mth, but little is known regarding the developmental functions of this receptor or any of its paralogs. We undertook a comprehensive analysis of developmental expression and sequence divergence in the mth/mthl gene family. Using in situ hybridization techniques, we detect expression of six genes (mthl1, 5, 9, 11, 13, and 14) in the embryo during gastrulation and development of the gut, heart, and lymph glands. Four receptors (mthl3, 4, 6, and 8) are expressed in the larval central nervous system, imaginal discs, or both, and two receptors (mthl10 and mth) are expressed in both embryos and larvae. Phylogenetic analysis of all mth/mthl genes in five Drosophila species, mosquito and flour beetle structured the mth/mthl family into several subclades. mthl1, 5, and 14 are present in most species, each forming a separate clade. A newly identified Drosophila mthl gene (CG31720; herein mthl15) formed another ancient clade. The remaining Drosophila receptors, including mth, are members of a large "superclade" that diversified relatively recently during dipteran evolution, in many cases within the melanogaster subgroup. Comparing the expression patterns of the mth/mthl "superclade" paralogs to the embryonic expression of the singleton ortholog in Tribolium suggests both subfunctionalization and acquisition of novel functionalities. Taken together, our findings shed novel light on mth as a young member of an adaptively evolving developmental gene family.     

Early gene interaction during prepupal expression of Drosophila arginine kinase

Arginine kinase displays a distinctive rise and fall in specific activity and specific protein levels during the prepupal stage of Drosophila development with maximal activity occurring at morphological stage P3. This developmentally regulated peak is under the influence of ecdysone. Altered doses of the major ecdysone-inducible “early” genes at cytological regions 75B and 2B5 alter this pattern of expression while altered doses of another major “early” gene at 74EF have no effect. We hypothesize that a product of the 2B5 locus and a product of the 75B locus interact to effect this developmental pattern of expression of Drosophila arginine kinase. © 1992 Wiley-Liss, Inc.     

Nucleotide polymorphism in the RpII215 gene region of the insular species Drosophila guanche: reduced efficacy of weak selection on synonymous variation

An approximately 6.9-kb region encompassing the RpII215 gene was sequenced for 24 individuals of the island endemic species Drosophila guanche. The comparative analysis of synonymous polymorphism and divergence in D. guanche and D. subobscura, two species with pronounced differences in population size, allows contrasting the nearly neutral character of synonymous mutations. In D. guanche, unlike in D. subobscura, (1) the ratio of preferred to unpreferred synonymous changes was similar for polymorphic and fixed changes, (2) the numbers of preferred and unpreferred changes, both polymorphic and fixed, could be explained by the mutational process, and (3) the estimated scaled selection coefficient for unpreferred mutations did not differ significantly from zero. Additionally, the comparative analysis revealed that both the ratio of preferred to unpreferred synonymous changes and the frequency spectrum of unpreferred polymorphic mutations differed significantly between species. All these results indicate that a large fraction of synonymous mutations in the RpII215 gene behave as effectively neutral in D. guanche, whereas they are weakly selected in D. subobscura. The reduced efficacy of selection in the insular species constitutes strong evidence of the nearly neutral character of synonymous mutations and, therefore, of the role of weak selection in maintaining codon bias.     

Shifting clinal patterns and microsatellite variation in Drosophila serrata populations: a comparison of populations near the southern border of the species range

Geographical patterns for quantitative traits in Drosophila and other insects are commonly used to investigate climatic selection. They are usually determined from comparisons of populations over extensive areas and based on one collection per population. Here we consider patterns in the Australian endemic species Drosophila serrata established over a shorter transect with repeated sampling. Summer (prewinter) and spring (post-winter) collections were made from 10 to 14 localities, incorporating the southern border of D.serrata and extending approximately 1000 km northwards along the eastern coast of Australia. Linear or curvilinear associations with latitude were evident for development time, viability and cold resistance but patterns differed between collections. Some geographical (population) and genetic associations between traits were found and these also tended to differ between collections. Results confirm the importance of cold stress resistance over winter to the southern border of this species. Microsatellite markers were developed for D.serrata. These indicated a low level of genetic differentiation between populations, high levels of gene flow and no evidence that the most southerly populations were isolated. The results suggest that selection generated geographical patterns in cold resistance, development time and viability, and that substantial gene flow may prevent adaptation at the border to conditions beyond the current distribution of D. serrata.     

Heritable variation in the attraction of Drosophila melanogaster to fruit in the field

Drosophila melanogaster were released at a field site and captured with two types of fruit pulp. When flies were rereleased they were more likely to be captured with the same type of fruit on which they were initially captured. Progeny reared in the laboratory tended to be attracted to the same type of fruit as their parents in field tests with two fruit combinations (lemon-orange, lemon-apple) but not a third combination (apple-orange). However, lines selected in the laboratory for increased attraction to apples or oranges over 15 generations differed in their response to these fruit types in the field. This indicates heritable variation for attraction to natural resources under field conditions. Simulations suggest that genotypes differed substantially in their responses to fruit resources.