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1.  Mating system variation drives rapid evolution of the female transcriptome in Drosophila pseudoobscura 
Ecology and Evolution  2014;4(11):2186-2201.
Interactions between the sexes are believed to be a potent source of selection on sex-specific evolution. The way in which sexual interactions influence male investment is much studied, but effects on females are more poorly understood. To address this deficiency, we examined gene expression in virgin female Drosophila pseudoobscura following 100 generations of mating system manipulations in which we either elevated polyandry or enforced monandry. Gene expression evolution following mating system manipulation resulted in 14% of the transcriptome of virgin females being altered. Polyandrous females elevated expression of a greater number of genes normally enriched in ovaries and associated with mitosis and meiosis, which might reflect female investment into reproductive functions. Monandrous females showed a greater number of genes normally enriched for expression in somatic tissues, including the head and gut and associated with visual perception and metabolism, respectively. By comparing our data with a previous study of sex differences in gene expression in this species, we found that the majority of the genes that are differentially expressed between females of the selection treatments show female-biased expression in the wild-type population. A striking exception is genes associated with male-specific reproductive tissues (in D. melanogaster), which are upregulated in polyandrous females. Our results provide experimental evidence for a role of sex-specific selection arising from differing sexual interactions with males in promoting rapid evolution of the female transcriptome.
PMCID: PMC4201433  PMID: 25360260
Drosophila; gene expression; microarray; polyandry; sexual selection
2.  Male-Specific Fruitless Isoforms Target Neurodevelopmental Genes to Specify a Sexually Dimorphic Nervous System 
Current Biology  2014;24(3):229-241.
In Drosophila, male courtship behavior is regulated in large part by the gene fruitless (fru). fru encodes a set of putative transcription factors that promote male sexual behavior by controlling the development of sexually dimorphic neuronal circuitry. Little is known about how Fru proteins function at the level of transcriptional regulation or the role that isoform diversity plays in the formation of a male-specific nervous system.
To characterize the roles of sex-specific Fru isoforms in specifying male behavior, we generated novel isoform-specific mutants and used a genomic approach to identify direct Fru isoform targets during development. We demonstrate that all Fru isoforms directly target genes involved in the development of the nervous system, with individual isoforms exhibiting unique binding specificities. We observe that fru behavioral phenotypes are specified by either a single isoform or a combination of isoforms. Finally, we illustrate the utility of these data for the identification of novel sexually dimorphic genomic enhancers and novel downstream regulators of male sexual behavior.
These findings suggest that Fru isoform diversity facilitates both redundancy and specificity in gene expression, and that the regulation of neuronal developmental genes may be the most ancient and conserved role of fru in the specification of a male-specific nervous system.
•Isoform-specific fru mutants reveal both functional redundancy and specificity•Fru isoform-specific genomic occupancy is characterized in the Drosophila nervous system•All Fru isoforms directly target neuronal morphogenesis genes•Isoform-specific motifs are associated with specific Fru isoform occupancy
Neville et al. characterize the roles of sex-specific Fruitless isoforms in specifying male behavior in Drosophila by generating novel isoform-specific mutants, along with using a genomic approach to identify direct Fruitless isoform targets during development.
PMCID: PMC3969260  PMID: 24440396
3.  Immune anticipation of mating in Drosophila: Turandot M promotes immunity against sexually transmitted fungal infections 
Although it is well known that mating increases the risk of infection, we do not know how females mitigate the fitness costs of sexually transmitted infections (STIs). It has recently been shown that female fruitflies, Drosophila melanogaster, specifically upregulate two members of the Turandot family of immune and stress response genes, Turandot M and Turandot C (TotM and TotC), when they hear male courtship song. Here, we use the Gal4/UAS RNAi gene knockdown system to test whether the expression of these genes provides fitness benefits for females infected with the entomopathogenic fungus, Metarhizium robertsii under sexual transmission. As a control, we also examined the immunity conferred by Dorsal-related immunity factor (Dif), a central component of the Toll signalling pathway thought to provide immunity against fungal infections. We show that TotM, but not TotC or Dif, provides survival benefits to females following STIs, but not after direct topical infections. We also show that though the expression of TotM provides fecundity benefits for healthy females, it comes at a cost to their survival, which helps to explain why TotM is not constitutively expressed. Together, these results show that the anticipatory expression of TotM promotes specific immunity against fungal STIs and suggest that immune anticipation is more common than currently appreciated.
PMCID: PMC3826220  PMID: 24174107
immune anticipation; sexually transmitted infections; ecological immunology; Drosophila melanogaster; Metarhizium robertsii; innate immunity
4.  4273π: Bioinformatics education on low cost ARM hardware 
BMC Bioinformatics  2013;14:243.
Teaching bioinformatics at universities is complicated by typical computer classroom settings. As well as running software locally and online, students should gain experience of systems administration. For a future career in biology or bioinformatics, the installation of software is a useful skill. We propose that this may be taught by running the course on GNU/Linux running on inexpensive Raspberry Pi computer hardware, for which students may be granted full administrator access.
We release 4273π, an operating system image for Raspberry Pi based on Raspbian Linux. This includes minor customisations for classroom use and includes our Open Access bioinformatics course, 4273π Bioinformatics for Biologists. This is based on the final-year undergraduate module BL4273, run on Raspberry Pi computers at the University of St Andrews, Semester 1, academic year 2012–2013.
4273π is a means to teach bioinformatics, including systems administration tasks, to undergraduates at low cost.
PMCID: PMC3751261  PMID: 23937194
Bioinformatics education; Teaching material; Raspberry Pi; Linux
5.  The genomic response to courtship song stimulation in female Drosophila melanogaster 
Courtship behaviour involves a complex exchange of signals and responses. These are usually studied at the phenotypic level, and genetic or transcriptional responses to courtship are still poorly understood. Here, we examine the gene-expression changes in Drosophila melanogaster females in response to one of the key male courtship signals in mate recognition, song produced by male wing vibration. Using long oligonucleotide microarrays, we identified several genes that responded differentially to the presence or absence of acoustic courtship stimulus. These changes were modest in both the number of genes involved and fold-changes, but notably dominated by antennal signalling genes involved in olfaction as well as neuropeptides and immune response genes. Second, we compared the expression patterns of females stimulated with synthetic song typical of either conspecific or heterospecific (Drosophila simulans) males. In this case, antennal olfactory signalling and innate immunity genes were also enriched among the differentially expressed genes. We confirmed and investigated the time course of expression differences of two identified immunity genes using real-time quantitative PCR. Our results provide novel insight into specific molecular changes in females in response to courtship song stimulation. These may be involved in both signal perception and interpretation and some may anticipate molecular interactions that occur between the sexes after mating.
PMCID: PMC3282362  PMID: 21976688
Drosophila melanogaster; gene expression; microarray; courtship song; Turandot
6.  Tissue-Specific Transcriptomics in the Field Cricket Teleogryllus oceanicus 
G3: Genes|Genomes|Genetics  2013;3(2):225-230.
Field crickets (family Gryllidae) frequently are used in studies of behavioral genetics, sexual selection, and sexual conflict, but there have been no studies of transcriptomic differences among different tissue types. We evaluated transcriptome variation among testis, accessory gland, and the remaining whole-body preparations from males of the field cricket, Teleogryllus oceanicus. Non-normalized cDNA libraries from each tissue were sequenced on the Roche 454 platform, and a master assembly was constructed using testis, accessory gland, and whole-body preparations. A total of 940,200 reads were assembled into 41,962 contigs, to which 36,856 singletons (reads not assembled into a contig) were added to provide a total of 78,818 sequences used in annotation analysis. A total of 59,072 sequences (75%) were unique to one of the three tissues. Testis tissue had the greatest proportion of tissue-specific sequences (62.6%), followed by general body (56.43%) and accessory gland tissue (44.16%). We tested the hypothesis that tissues expressing gene products expected to evolve rapidly as a result of sexual selection—testis and accessory gland—would yield a smaller proportion of BLASTx matches to homologous genes in the model organism Drosophila melanogaster compared with whole-body tissue. Uniquely expressed sequences in both testis and accessory gland showed a significantly lower rate of matching to annotated D. melanogaster genes compared with those from general body tissue. These results correspond with empirical evidence that genes expressed in testis and accessory gland tissue are rapidly evolving targets of selection.
PMCID: PMC3564983  PMID: 23390599
field cricket; gryllid; reference transcriptome; Teleogryllus oceanicus; tissue-specific transcriptome
7.  Introduction. Speciation in plants and animals: pattern and process 
Although approximately 150 years have passed since the publication of On the origin of species by means of natural selection, the definition of what species are and the ways in which species originate remain contentious issues in evolutionary biology. The biological species concept, which defines species as groups of interbreeding natural populations that are reproductively isolated from other such groups, continues to draw support. However, there is a growing realization that many animal and plant species can hybridize with their close relatives and exchange genes without losing their identity. On occasion, such hybridization can lead to the origin of new species. A key to understanding what species are and the ways in which they originate rests to a large extent on a detailed knowledge of the nature and genetics of factors that limit gene flow between species and the conditions under which such isolation originates. The collection of papers in this issue addresses these topics and deals as well with some specific issues of hybrid speciation and the causes of species radiations. The papers included arise from a 1-day symposium on speciation held during the Sixth Biennial Meeting of the Systematics Association at Edinburgh in August 2007. In this introduction, we provide some background to these papers and highlight some key points made. The papers make clear that highly significant advances to our understanding of animal and plant speciation are currently being made across the range of this topic.
PMCID: PMC2459220  PMID: 18583278
speciation; species concepts; reproductive isolation; hybridization; species radiations
8.  Incipient speciation in Drosophila melanogaster involves chemical signals 
Scientific Reports  2012;2:224.
The sensory and genetic bases of incipient speciation between strains of Drosophila melanogaster from Zimbabwe and those from elsewhere are unknown. We studied mating behaviour between eight strains – six from Zimbabwe, together with two cosmopolitan strains. The Zimbabwe strains showed significant sexual isolation when paired with cosmopolitan males, due to Zimbabwe females discriminating against these males. Our results show that flies' cuticular hydrocarbons (CHs) were involved in this sexual isolation, but that visual and acoustic signals were not. The mating frequency of Zimbabwe females was highly significantly negatively correlated with the male's relative amount of 7-tricosene (%7-T), while the mating of cosmopolitan females was positively correlated with %7-T. Variation in transcription levels of two hydrocarbon-determining genes, desat1 and desat2, did not correlate with the observed mating patterns. Our study represents a step forward in our understanding of the sensory processes involved in this classic case of incipient speciation.
PMCID: PMC3261631  PMID: 22355738
9.  Sexual selection on song and cuticular hydrocarbons in two distinct populations of Drosophila montana 
Ecology and Evolution  2012;2(1):80-94.
Sexual selection has the potential to contribute to population divergence and speciation. Most studies of sexual selection in Drosophila have concentrated on a single signaling modality, usually either courtship song or cuticular hydrocarbons (CHCs), which can act as contact pheromones. We have examined the relationship between both signal types and reproductive success using F1–3 offspring of wild-collected flies, raised in the lab. We used two populations of the Holarctic species Drosophila montana that represent different phylogeographic clades that have been separate for ca. 0.5 million years (MY), and differ to some extent in both traits. Here, we characterize the nature and identify the targets of sexual selection on song, CHCs, and both traits combined within the populations. Three measures of courtship outcome were used as fitness proxies. They were the probability of mating, mating latency, and the production of rejection song by females, and showed patterns of association with different traits that included both linear and quadratic selection. Courtship song predicted courtship outcome better than CHCs and the signal modalities acted in an additive rather than synergistic manner. Selection was generally consistent in direction and strength between the two populations and favored males that sang more vigorously. Sexual selection differed in the extent, strength, and nature on some of the traits between populations. However, the differences in the directionality of selection detected were not a good predictor of population differences. In addition, a character previously shown to be important for species recognition, interpulse interval, was found to be under sexual selection. Our results highlight the complexity of understanding the relationship between within-population sexual selection and population differences. Sexual selection alone cannot predict differences between populations.
PMCID: PMC3297180  PMID: 22408728
Courtship song; cuticular hydrocarbons; Drosophila montana; selection analysis; sexual selection
10.  Sexual and postmating reproductive isolation between allopatric Drosophila montana populations suggest speciation potential 
Widely distributed species with populations adapted to different environmental conditions can provide valuable opportunities for tracing the onset of reproductive incompatibilities and their role in the speciation process. Drosophila montana, a D. virilis group species found in high latitude boreal forests in Nearctic and Palearctic regions around the globe, could be an excellent model system for studying the early stages of speciation, as a wealth of information concerning this species' ecology, mating system, life history, genetics and phylogeography is available. However, reproductive barriers between populations have hereto not been investigated.
We report both pre- and postmating barriers to reproduction between flies from European (Finnish) and North American (Canadian) populations of Drosophila montana. Using a series of mate-choice designs, we show that flies from these two populations mate assortatively (i.e., exhibit significant sexual isolation) while emphasizing the importance of experimental design in these kinds of studies. We also assessed potential postmating isolation by quantifying egg and progeny production in intra- and interpopulation crosses and show a significant one-way reduction in progeny production, affecting both male and female offspring equally.
We provide evidence that allopatric D. montana populations exhibit reproductive isolation and we discuss the potential mechanisms involved. Our data emphasize the importance of experimental design in studies on premating isolation between recently diverged taxa and suggest that postmating barriers may be due to postcopulatory-prezygotic mechanisms. D. montana populations seem to be evolving multiple barriers to gene flow in allopatry and our study lays the groundwork for future investigations of the genetic and phenotypic mechanisms underlying these barriers.
PMCID: PMC3065424  PMID: 21396136
11.  Sites of evolutionary divergence differ between olfactory and gustatory receptors of Drosophila 
Biology Letters  2009;5(2):244-247.
Drosophila olfactory (ORs) and gustatory (GRs) receptors are evolutionarily unrelated to vertebrate ORs or nematode chemosensory receptors. Insect ORs display a reverse membrane topology compared with conventional G-protein-coupled receptors, suggesting that the mammalian scheme of chemosensory signal transduction cannot directly apply to insects. Experimental studies of GR membrane topology are lacking. We analysed the distribution of amino acid sites in GRs and ORs that show evidence for divergence under either positive selection or relaxed purifying constraints, in the genomes of 12 Drosophila species and found significant differences between these two receptor types. This suggests that insect ORs and GRs have distinct molecular properties and mechanisms of ligand recognition and/or signal transduction.
PMCID: PMC2665830  PMID: 19141414
gustatory receptors; olfactory receptors; Drosophila; divergent selection
12.  Evolution of a Complex Locus: Exon Gain, Loss and Divergence at the Gr39a Locus in Drosophila 
PLoS ONE  2008;3(1):e1513.
Gene families typically evolve by gene duplication followed by the adoption of new or altered gene functions. A different way to evolve new but related functions is alternative splicing of existing exons of a complex gene. The chemosensory gene families of animals are characterised by numerous loci of related function. Alternative splicing has only rarely been reported in chemosensory loci, for example in 5 out of around 120 loci in Drosophila melanogaster. The gustatory receptor gene Gr39a has four large exons that are alternatively spliced with three small conserved exons. Recently the genome sequences of eleven additional species of Drosophila have become available allowing us to examine variation in the structure of the Gr39a locus across a wide phylogenetic range of fly species.
Methodology/Principal Findings
We describe a fifth exon and show that the locus has a complex evolutionary history with several duplications, pseudogenisations and losses of exons. PAML analyses suggested that the whole gene has a history of purifying selection, although this was less strong in exons which underwent duplication.
Estimates of functional divergence between exons were similar in magnitude to functional divergence between duplicated genes, suggesting that exon divergence is broadly equivalent to gene duplication.
PMCID: PMC2204066  PMID: 18231599
13.  Positive assortative mating between recently described sympatric morphs of Icelandic sticklebacks 
Biology Letters  2006;2(2):250-252.
Recently, models of sympatric speciation have suggested that assortative mating can develop between sympatric morphs due to divergence in an ecologically important character. For example, in sympatric pairs of threespine stickleback (Gasterosteus aculeatus L.) size-assortative mating seems to be instrumental in reproductive isolation. Here, we examine courtship behaviour and assortative mating of newly described sympatric stickleback morphs in Lake Thingvallavatn, Iceland. We find that the two morphs show strong positive assortative mating. However, the mechanism involved in mate choice does not seem to be as straightforward as in other similar systems of sympatric stickleback morphs and may involve variation in nest type.
PMCID: PMC1618888  PMID: 17148375
speciation; assortative mating; stickleback
14.  Multiple differences in calling songs and other traits between solitary and gregarious Mormon crickets from allopatric mtDNA clades 
In acoustic species, traits such as male calling song are likely to diverge quickly between allopatric populations due to sexual selection, and divergence in parameters such as carrier frequency, chirp structure, and other important song characters can influence sexual isolation. Here we make use of two forms of Mormon crickets to examine differences in a broad suite of traits that have the potential to influence speciation via sexual isolation. Mormon crickets in "gregarious" populations aggregate into dense migratory bands, and females are the sexually competitive sex (sex-role reversal). There is also a non-outbreak "solitary" form. These two forms are largely but not perfectly correlated with a significant mtDNA subdivision within the species that is thought to have arisen in allopatry. Combined information about multiple, independently evolving traits, such as morphology and structural and behavioural differences in calling song, provides greater resolution of the overall differences between these allopatric populations, and allows us to assess their stage of divergence. We test two predictions, first that the forms differ in song and second that gregarious males are more reluctant to sing than solitary males due to sex role reversal. We also tested for a difference in the relationship between the size of the forewing resonator, the mirror, and carrier frequency, as most models of sound production in crickets indicate that mirror size should predict carrier frequency.
Multivariate analyses showed that solitary and gregarious individuals from different populations representing the two mtDNA clades had almost non-overlapping distributions based on multiple song and morphological measurements. Carrier frequency differed between the two, and gregarious males were more reluctant to sing overall. Mirror size predicted carrier frequency; however, the relationship between mirror size and surface area varied between solitary and gregarious forms, suggesting that factors above and beyond mirror size contribute to carrier frequency.
The two clades of Mormon crickets differ in a broad suite of independent traits that probably justify subspecies status (the two can successfully mate so may not be reproductively isolated). However, our results emphasize the importance of carefully distinguishing the ultimate causation of differences between traits used to delineate species or subspecies boundaries.
PMCID: PMC1790887  PMID: 17241474
15.  Nonlinear and correlational sexual selection on 'honest' female ornamentation. 
Female ornamentation has long been overlooked because of the greater prevalence of elaborate displays in males. However, the circumstances under which females would benefit from honestly signalling their quality are limited. Females are not expected to invest in ornamentation unless the fitness benefits of the ornament exceed those derived from investing the resources directly into offspring. It has been proposed that when females gain direct benefits from mating, females may instead be selected for ornamentation that deceives males about their reproductive state. In the empidid dance flies, males frequently provide nuptial gifts and it is usually only the female that is ornamented. Female traits in empidids, such as abdominal sacs and enlarged pinnate leg scales, have been proposed to 'deceive' males into matings by disguising egg maturity. We quantified sexual selection in the dance fly Rhamphomyia tarsata and found escalating, quadratic selection on pinnate scales and that pinnate scales honestly reflect female fecundity. Mated females had a larger total number and more mature eggs than unmated females, highlighting a potential benefit rather than a cost of male mate choice. We also show correlational selection on female pinnate scales and fecundity. Correlational selection, equivalent investment patterns or increased nutrition from nuptial gifts may all maintain honesty in female ornamentation.
PMCID: PMC1691484  PMID: 14561280
Sexual selection is predicted to drive the coevolution of mating signals and preferences (mating traits) within populations, and could play a role in speciation if sexual isolation arises due to mating trait divergence between populations. However, few studies have demonstrated that differences in mating traits between populations result from sexual selection alone. Experimental evolution is a promising approach to directly examine the action of sexual selection on mating trait divergence among populations. We manipulated the opportunity for sexual selection (low vs. high) in populations of Drosophila pseudoobscura. Previous studies on these experimental populations have shown that sexual selection manipulation resulted in the divergence between sexual selection treatments of several courtship song parameters, including interpulse interval (IPI) which markedly influences male mating success. Here, we measure female preference for IPI using a playback design to test for preference divergence between the sexual selection treatments after 130 generations of experimental sexual selection. The results suggest that female preference has coevolved with male signal, in opposite directions between the sexual selection treatments, providing direct evidence of the ability of sexual selection to drive the divergent coevolution of mating traits between populations. We discuss the implications in the context sexual selection and speciation.
PMCID: PMC4262321  PMID: 24931497
Coevolution; courtship song; Drosophila; experimental evolution; population divergence; speciation

Results 1-16 (16)