Elsevier

Current Opinion in Insect Science

Volume 31, February 2019, Pages 131-138
Current Opinion in Insect Science

Detoxifying enzyme complements and host use phenotypes in 160 insect species

https://doi.org/10.1016/j.cois.2018.12.008Get rights and content

Highlights

  • 160 insect genomes screened for esterase, GST and cytochrome P450 genes.

  • Omnivores and herbivores eating chemically complex tissues have many of these genes.

  • Species using chemically simpler tissues such as sap, nectar and blood have relatively few.

  • Polyphages have more than other species using the same tissue type.

We use the genomes of 160 insect species to test the hypothesis that the size of detoxifying enzyme families is greater in species using more chemically diverse food resources. Phylogenetically appropriate contrasts in subsamples of the data generally support the hypothesis. We find relatively high numbers of cytochrome P450, glutathione S-transferase and carboxyl/choline esterase genes in omnivores and herbivores feeding on chemically complex tissues and relatively low numbers of these genes in specialists on relatively simple diets, including plant sap, nectar and pollen, and blood. Among Lepidoptera feeding on green plant tissue and Condylognatha feeding on sap we also find more of these genes in highly polyphagous species, many of which are major agricultural pests. These genomic signatures of food resource use are consistent with the hypothesis that some taxa are preadapted for insecticide resistance evolution.

Introduction

Abundant evidence has accumulated over the last 50 years showing that the ability of insect herbivores to detoxify plant allelochemicals affects their ability to utilize different plant hosts, both in terms of the type of host tissue and the range of host species they will use [1, 2, 3, 4]. This has stimulated several attempts over the last 15 years to compare the genomic complements of the gene families chiefly responsible for the transport and detoxification of xenobiotics in insects that differ in host use. Early studies of this sort found unusually low numbers of cytochrome P450 (P450), carboxyl/choline esterase (CCE) and glutathione S-transferase (GST) genes in two feeding specialists, the honeybee Apis mellifera [5] and body louse Pediculus humanus [6], suggesting that there may indeed be a relationship between the number of detoxifying gene/enzyme systems in the insect and the allelochemical diversity of its hosts/food sources.

Three specific predictions follow from this proposition. First, omnivores using both plant and animal food resources should have more such genes than carnivores and herbivores. Second, polyphages with a broad host range should have more such genes than those confined to one or a few host species. Third, insects using host tissues with complex secondary chemistry such as green plant tissues should have more of these genes than those using tissues with simpler defense chemistry such as nectar, sap or blood.

The first large scale comparative genomic investigation of these issues, involving 65 herbivorous species, found only equivocal evidence in support of these predictions [7••]; the 65 species were too sparsely distributed across insect orders and host use types to provide a robust test. However subsequent work on the Lepidoptera and Diptera has supported two of the predictions while also indicating some additional complexities. In the case of the Lepidoptera, data on four additional highly polyphagous species [8, 9, 10] generated a data set of eleven species that all utilize green plant tissue and showed a positive relationship between the number of genes in the three families and host range. In the case of the Diptera, an analysis of the above three gene families plus the ATP-binding cassette transporters (ABCs) and the UDP-glycosyl transferases (UGTs) which are now also clearly implicated in allelochemical detoxification [11,12] across 14 Drosophila species [13,14] found that certain species living on fresh fruit or the highly toxic Morinda citrifolia fruit have relatively high numbers of CCEs, GSTs, P450s, and UGTs, while the ABCs are most numerous in the flower-feeding specialist Drosophila elegans and the food source generalist Drosophila hydei.

Given these recent findings and the expanding availability of genomes, this paper revisits the approach of Rane et al. [7••], this time applying it to 160 appropriate genomes.

Section snippets

Data sources and analytical methods

Our analysis is largely based on six lineages of Insecta: the Coleoptera (nine species), Condylognatha (comprising 15 Hemiptera and one Thysanoptera), Diptera (66 species), the ants and other (mainly basal) Hymenoptera (20 and 26 respectively) and Lepidoptera (20 species). We also include data for two species of Blattodea and one species each of Neoptera and Odonata in certain analyses. Complete genome sequences and annotations for all the above species were obtained from NCBI (//www.ncbi.nlm.nih.gov

Conclusions

Compared to our earlier work using just 65 species [7••], the current analysis, particularly around predictions one and three, provides stronger support for the hypothesis of a positive association between the size of insects’ repertoire of detoxification genes and the extent of secondary chemistry defenses in their hosts. Perhaps the clearest evidence comes from the high gene counts for omnivores and for herbivores using more chemically complex plant tissue diets, and the relatively low counts

Conflict of interest statement

Nothing declared.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Stephen Richards and Hugh Robertson for pre-publication access to genome data for i5k species and Diachasma alloeum.

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