In insects, species comparisons suggest a weak association between upper thermal limits and latitude in contrast to a stronger association for lower limits. To compare this to latitudinal patterns of thermal responses within species, we considered latitudinal variation in heat and cold resistance in Drosophila melanogaster. We found opposing clines in resistance to these temperature extremes in comparisons of 17-24 populations from coastal eastern Australia. Knockdown time following heat shock increased towards the tropics, whereas recovery time following cold shock decreased towards temperate latitudes. Mortality following cold shock also showed a clinal pattern. Clinal associations with latitude were linear and related to minimum temperatures in the coldest month (for cold resistance) and maximum temperatures in the warmest month (for heat resistance). This suggests that within species both high and low temperature responses can vary with latitude as a consequence of direct or indirect effects of selection.
Emergence of polyphagous herbivorous insects entails significant adaptation to recognize, detoxify and digest a variety of host-plants. Despite of its biological and practical importance - since insects eat 20% of crops - no exhaustive analysis of gene repertoires required for adaptations in generalist insect herbivores has previously been performed. The noctuid moth Spodoptera frugiperda ranks as one of the world’s worst agricultural pests. This insect is polyphagous while the majority of other lepidopteran herbivores are specialist. It consists of two morphologically indistinguishable strains (“C” and “R”) that have different host plant ranges. To describe the evolutionary mechanisms that both enable the emergence of polyphagous herbivory and lead to the shift in the host preference, we analyzed whole genome sequences from laboratory and natural populations of both strains. We observed huge expansions of genes associated with chemosensation and detoxification compared with specialist Lepidoptera. These expansions are largely due to tandem duplication, a possible adaptation mechanism enabling polyphagy. Individuals from natural C and R populations show significant genomic differentiation. We found signatures of positive selection in genes involved in chemoreception, detoxification and digestion, and copy number variation in the two latter gene families, suggesting an adaptive role for structural variation.
Background Helicoverpa armigera and Helicoverpa zea are major caterpillar pests of Old and New World agriculture, respectively. Both, particularly H. armigera, are extremely polyphagous, and H. armigera has developed resistance to many insecticides. Here we use comparative genomics, transcriptomics and resequencing to elucidate the genetic basis for their properties as pests.ResultsWe find that, prior to their divergence about 1.5 Mya, the H. armigera/H. zea lineage had accumulated up to more than 100 more members of specific detoxification and digestion gene families and more than 100 extra gustatory receptor genes, compared to other lepidopterans with narrower host ranges. The two genomes remain very similar in gene content and order, but H. armigera is more polymorphic overall, and H. zea has lost several detoxification genes, as well as about 50 gustatory receptor genes. It also lacks certain genes and alleles conferring insecticide resistance found in H. armigera. Non-synonymous sites in the expanded gene families above are rapidly diverging, both between paralogues and between orthologues in the two species. Whole genome transcriptomic analyses of H. armigera larvae show widely divergent responses to different host plants, including responses among many of the duplicated detoxification and digestion genes.ConclusionsThe extreme polyphagy of the two heliothines is associated with extensive amplification and neofunctionalisation of genes involved in host finding and use, coupled with versatile transcriptional responses on different hosts. H. armigera’s invasion of the Americas in recent years means that hybridisation could generate populations that are both locally adapted and insecticide resistant.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-017-0402-6) contains supplementary material, which is available to authorized users.
Olfaction plays an important role in the life history of insects, including key behaviours such as host selection, oviposition and mate recognition. Odour perception by insects is primarily mediated by the large diverse family of odourant receptors (Ors) that are expressed on the dendrites of olfactory neurones housed within chemosensilla. However, few Or sequences have been identified from the Lepidoptera, an insect order that includes some of the most important pest species worldwide. We have identified 41 Or gene sequences from the silkworm (Bombyx mori) genome, more than double the number of published Or sequences from the Lepidoptera. Many silkworm Ors appear to be orthologs of the 17 published tobacco budworm (Heliothis virescens) Ors indicating that many Or lineages may be conserved within the Lepidoptera. The majority of the Or genes are expressed in adult female and male antennae (determined by quantitative real-time PCR analysis), supporting their probable roles in adult olfaction. Several Or genes are expressed at high levels in both male and female antennae, suggesting they mediate the perception of common host or conspecific volatiles important to both sexes. BmOrs 45-47 group together in the same phylogenetic branch and all three are expressed at moderate female-biased ratios, six to eight times higher in female compared to male moth antennae. Interestingly, BmOrs19 and 30 appear to be expressed predominantly in female antennae, opposite to that of the published silkworm pheromone receptors BmOrs 1 and 3 that are specific to male antennae. These results suggest that BmOr19 and 30 may detect odours critical to female behaviour, such as oviposition cues or male-produced courtship pheromones.
Drosophila melanogaster occurs in diverse climatic regions and shows opposing clinal changes in resistance to heat and resistance to cold along a 3000 km latitudinal transect on the eastern coast of Australia. We report here on variation at a polymorphic 8 bp-indel site in the heat shock hsr-omega gene that maps to the right arm of chromosome 3. The frequency of the genetic element marked by the L form of the gene was strongly and positively associated with latitude along this transect, and latitudinal differences in L frequency were robustly associated with latitudinal differences in maximum temperature for the hottest month. On a genetic background mixed for genes from each end of the cline a set of 10 lines was derived, five of which were fixed for the L marker, the absence of In(3R)P and 12 kb of repeats at a second polymorphic site at the 3 0 end of hsr-omega, and five that were fixed for the S marker, In(3R)P and 15 kb of hsromega repeats. For two different measures of heat tolerance S lines outperformed L lines, and for two different measures of cold tolerance L lines outperformed S lines. These data suggest that an element on the right arm of chromosome 3, possibly In(3R)P, confers heat resistance but carries the trade-off of also conferring susceptibility to cold. This element occurs at high frequency near the equator. The alternate element on the other hand, at high frequency at temperate latitudes, confers cold resistance at the cost of heat susceptibility.
Resistance to low temperatures can vary markedly among invertebrate species and is directly related to their distribution. Despite the ecological importance of cold resistance this trait has rarely been studied genetically, mainly because low and variable fitness of offspring from cold-stressed mothers makes it difficult to undertake selection experiments and compare cold resistance of parents and offspring. One measure of cold resistance that varies geographically in Drosophila melanogaster and that is amenable to genetic analysis is chill-coma recovery. Three replicate lines of D. melanogaster were selected every second generation, for over 30 generations, for decreased recovery time following exposure to 0 degrees C. Correlated responses were scored to characterize underlying physiological traits and to investigate interactions with other traits. Lines responded rapidly to the intermittent selection regime with realized heritabilities varying from 33% to 46%. Selected lines showed decreased recovery time after exposure to a broad range of low temperatures and also had a lower mortality following a more severe cold shock, indicating that a general mechanism underlying cold resistance had been selected. The selection response was independent of plastic changes in cold resistance because the selected lines maintained their ability to harden (i.e. a short-term exposure to cool temperature resulted in decreased recovery time in subsequent chill-coma assays). Changes in cold resistance were not associated with changes in resistance to high temperature exposure, and selected lines showed no changes in wing size, development time or viability. However, there was a decrease in longevity in the selected lines due to an earlier onset of ageing. These results indicate that chill-coma recovery can be rapidly altered by selection, as long as selection is undertaken every second generation to avoid carry-over effects, and suggest that lower thermal limits can be shifted towards increased cold resistance independently of upper thermal limits and without tradeoffs in many life-history traits.
Insect gustatory receptors are predicted to have a seven-transmembrane structure and are distantly related to insect olfactory receptors, which have an inverted topology compared with G-protein coupled receptors, including mammalian olfactory receptors. In contrast, the topology of insect gustatory receptors remains unknown. Except for a few examples from Drosophila, the specificity of individual insect gustatory receptors is also unknown. In this study, the total number of identified gustatory receptors in Bombyx mori was expanded from 65 to 69. BmGr8, a silkmoth gustatory receptor from the sugar receptor subfamily, was expressed in insect cells. Membrane topology studies on BmGr8 indicate that, like insect olfactory receptors, it has an inverted topology relative to G protein-coupled receptors. An orphan GR from the bitter receptor family, BmGr53, yielded similar results. We infer, from the finding that two distantly related BmGrs have an intracellular N-terminus and an odd number of transmembrane spans, that this is likely to be a general topology for all insect gustatory receptors. We also show that BmGr8 functions independently in Sf9 cells and responds in a concentration-dependent manner to the polyalcohols myo-inositol and epi-inositol but not to a range of mono- and di-saccharides. BmGr8 is the first chemoreceptor shown to respond specifically to inositol, an important or essential nutrient for some Lepidoptera. The selectivity of BmGr8 responses is consistent with the known responses of one of the gustatory receptor neurons in the lateral styloconic sensilla of B. mori, which responds to myo-inositol and epi-inositol but not to allo-inositol.
Clinal variation has been described in a number of inversions in Drosophila but these clines are often characterized by cytological techniques using small sample sizes, and associations with specific genes are rarely considered. Here we have developed a molecular assay for In(3R)Payne in Drosophila melanogaster from eastern Australia populations. It shows in repeated samples that the inversion cline is very tightly associated with latitude and is almost fixed in tropical populations while relatively rare in temperate populations. This steep cline has shifted in position in the last 20 years. The heat shock gene, hsr-omega, located centrally inside the inversion sequence, shows a different clinal pattern to In(3R)Payne. These results suggest strong ongoing selection on In(3R)Payne over the last 100 years since the colonization of Australia that is partly independent of hsr-omega.
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