The insect chemoreceptor superfamily comprises the olfactory receptor (Or) and gustatory receptor (Gr) multigene families. These families give insects the ability to smell and taste chemicals in the environment and are thus rich resources for linking molecular evolutionary and ecological processes. Although dramatic differences in family size among distant species and high divergence among paralogs have led to the belief that the two families evolve rapidly, a lack of evolutionary data over short time scales has frustrated efforts to identify the major forces shaping this evolution. Here, we investigate patterns of gene loss/gain, divergence, and polymorphism in the entire repertoire of ∼130 chemoreceptor genes from five closely related species of Drosophila that share a common ancestor within the past 12 million years. We demonstrate that the overall evolution of the Or and Gr families is nonneutral. We also show that selection regimes differ both between the two families as wholes and within each family among groups of genes with varying functions, patterns of expression, and phylogenetic histories. Finally, we find that the independent evolution of host specialization in Drosophila sechellia and D. erecta is associated with a fivefold acceleration of gene loss and increased rates of amino acid evolution at receptors that remain intact. Gene loss appears to primarily affect Grs that respond to bitter compounds while elevated Ka/Ks is most pronounced in the subset of Ors that are expressed in larvae. Our results provide strong evidence that the observed phenomena result from the invasion of a novel ecological niche and present a unique synthesis of molecular evolutionary analyses with ecological data.

Reference collections of multiple Drosophila lines with accumulating collections of "omics" data have proven especially valuable for the study of population genetics and complex trait genetics. Here we present a description of a resource collection of 84 strains of Drosophila melanogaster whose genome sequences were obtained after 12 generations of full-sib inbreeding. The initial rationale for this resource was to foster development of a systems biology platform for modeling metabolic regulation, using natural polymorphisms as perturbations. As reference lines, they are amenable to repeated phenotypic measurements, and already a large collection of metabolic traits have been assayed. Another key feature of these strains is their widespread geographic origin, coming from Beijing, Ithaca, Netherlands, Tasmania and Zimbabwe. After obtaining 12.5x coverage of paired-end Illumina sequence reads, SNP and indel calls were made with the GATK platform. Thorough quality control was enabled by deep sequencing one line to >100x, and SNPs and indels were validated using ddRAD-sequencing as an orthogonal platform. In addition, a series of preliminary population genetic tests were performed with these SNP data for assessment of data quality. We found 83 segregating inversions among the lines, and as expected these were especially abundant in the African sample. We anticipate that this will make a useful addition to the set of reference D. melanogaster strains, thanks to its geographic structuring and unusually high level of genetic diversity.

Drosophila sechellia, a species closely related to the model species Drosophila melanogaster, bypasses a premature stop codon in neuronal cells to express a functional olfactory receptor protein from an assumed pseudogene template. Pseudogenes—genes that have accumulated premature termination codons (PTC)—are considered 'junk' DNA. They may produce regulatory RNAs or small polypeptidic fragments but no functional protein, or so it was thought. Here Richard Benton and colleagues report that the Ir75a pseudogene in Drosophila sechelia encodes a functional olfactory receptor as a consequence of efficient translational read-through of its PTC, exclusively in neurons. The authors go on to identify several other such 'pseudo-pseudogenes' that act as functional genes despite PTCs, among different olfactory receptor families and various species, which suggests that genome annotation should be reconsidered, especially with respect to PTC-containing disease genes. Pseudogenes are generally considered to be non-functional DNA sequences that arise through nonsense or frame-shift mutations of protein-coding genes1. Although certain pseudogene-derived RNAs have regulatory roles2, and some pseudogene fragments are translated3, no clear functions for pseudogene-derived proteins are known. Olfactory receptor families contain many pseudogenes, which reflect low selection pressures on loci no longer relevant to the fitness of a species4. Here we report the characterization of a pseudogene in the chemosensory variant ionotropic glutamate receptor repertoire5,6 of Drosophila sechellia, an insect endemic to the Seychelles that feeds almost exclusively on the ripe fruit of Morinda citrifolia7. This locus, D. sechellia Ir75a, bears a premature termination codon (PTC) that appears to be fixed in the population. However, D. sechellia Ir75a encodes a functional receptor, owing to efficient translational read-through of the PTC. Read-through is detected only in neurons and is independent of the type of termination codon, but depends on the sequence downstream of the PTC. Furthermore, although the intact Drosophila melanogaster Ir75a orthologue detects acetic acid—a chemical cue important for locating fermenting food8,9 found only at trace levels in Morinda fruit10—D. sechellia Ir75a has evolved distinct odour-tuning properties through amino-acid changes in its ligand-binding domain. We identify functional PTC-containing loci within different olfactory receptor repertoires and species, suggesting that such ‘pseudo-pseudogenes’ could represent a widespread phenomenon.

Amino acids are important nutrients for animals, reflected in conserved internal pathways in vertebrates and invertebrates for monitoring cellular levels of these compounds. In mammals, sensory cells and metabotropic glutamate receptor-related taste receptors that detect environmental sources of amino acids in food are also well-characterised. By contrast, it is unclear how insects perceive this class of molecules through peripheral chemosensory mechanisms. Here we investigate amino acid sensing in Drosophila melanogaster larvae, which feed ravenously to support their rapid growth. We show that larvae display diverse behaviours (attraction, aversion, neutral) towards different amino acids, which depend upon stimulus concentration. Some of these behaviours require IR76b, a member of the variant ionotropic glutamate receptor repertoire of invertebrate chemoreceptors. IR76b is broadly expressed in larval taste neurons, suggesting a role as a co-receptor. We identify a subpopulation of these neurons that displays physiological activation by some, but not all, amino acids, and which mediate suppression of feeding by high concentrations of at least a subset of these compounds. Our data reveal the first elements of a sophisticated neuronal and molecular substrate by which these animals detect and behave towards external sources of amino acids.

Few studies have influenced thought on the nature of sexual selection to the extent of the classic paper of A. J. Bateman on mating patterns in Drosophila. However, interpretation of his study remains controversial, and a lack of modern empirical evidence prevents a consensus with respect to the perceived utility of Bateman's principles in the study of sexual selection. Here, we use a genetic study of natural mating patterns in the rough–skinned newt, Taricha granulosa, to investigate the concordance between Bateman's principles and the intensity of sexual selection. We found that males experienced strong sexual selection on tail height and body size, while sexual selection was undetectable in females. This direct quantification of sexual selection agreed perfectly with inferences that are based on Bateman's principles. Specifically, males (in comparison with females) exhibited greater standardized variances in reproductive and mating success, as well as a stronger relationship between mating success and reproductive success. Overall, our results illustrate that Bateman's principles provide the only quantitative measures of the mating system with explicit connections to formal selection theory and should be the central focus of studies of mating patterns in natural populations.