Genomic footprint of evolution of eusociality in bees: floral food use and CYPome “blooms”

Harpur, Brock A.; Dogantzis, Kathleen A.; Zayed, Amro; Berenbaum, May R.

doi:10.1007/s00040-018-0631-x

Cited by 32 publications

(56 citation statements)

References 41 publications

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“…A rapid birth–death model of evolution is characteristic of xenobiotic-metabolizing P450s, in contrast to P450s with endogenous functions [18], and the expansion of the CYP9Q subfamily in social bees may have occurred to allow xenobiotics specifically associated with this life history to be detoxified. In relation to this, recent analysis of the CYPomes of ten bee species has suggested that the expansion of the CYP6AS subfamily in perennial eusocial bees resulted from increased exposure to phytochemcials, as a result of the concentration of nectar into honey, pollen into beebread and plant resins into propolis [19].…”

Section: Discussionmentioning

confidence: 99%

Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis

et al. 2019

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The impact of pesticides on the health of bee pollinators is determined in part by the capacity of bee detoxification systems to convert these compounds to less toxic forms. For example, recent work has shown that cytochrome P450s of the CYP9Q subfamily are critically important in defining the sensitivity of honey bees and bumblebees to pesticides, including neonicotinoid insecticides. However, it is currently unclear if solitary bees have functional equivalents of these enzymes with potentially serious implications in relation to their capacity to metabolise certain insecticides. To address this question, we sequenced the genome of the red mason bee, Osmia bicornis , the most abundant and economically important solitary bee species in Central Europe. We show that O . bicornis lacks the CYP9Q subfamily of P450s but, despite this, exhibits low acute toxicity to the N -cyanoamidine neonicotinoid thiacloprid. Functional studies revealed that variation in the sensitivity of O . bicornis to N -cyanoamidine and N -nitroguanidine neonicotinoids does not reside in differences in their affinity for the nicotinic acetylcholine receptor or speed of cuticular penetration. Rather, a P450 within the CYP9BU subfamily, with recent shared ancestry to the Apidae CYP9Q subfamily, metabolises thiacloprid in vitro and confers tolerance in vivo . Our data reveal conserved detoxification pathways in model solitary and eusocial bees despite key differences in the evolution of specific pesticide-metabolising enzymes in the two species groups. The discovery that P450 enzymes of solitary bees can act as metabolic defence systems against certain pesticides can be leveraged to avoid negative pesticide impacts on these important pollinators.

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Section: Discussionmentioning

confidence: 99%

Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis

et al. 2019

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“…Genomic comparisons among anciently evolved herbivores and distantly related non-herbivores, or across herbivorous lineages, have uncovered striking expansions and losses of genes involved in chemosensation and detoxification in arthropods (e.g., (19,32,65,69,70) . Yet the lack of dense sampling among closely related taxa has, in many cases, precluded pinpointing the timing of these changes relative to the evolution of herbivory.…”

Section: Discussionmentioning

confidence: 99%

“…However, new studies suggest that this finding obscures potentially adaptive "blooms" that are more nuanced, localized phylogenetically and driven by the particular niches of the insects involved. Specifically, studies on insects with well-defined interactions with plants, including shifts from carnivory to folivory in bees and variation in diet breadth across Drosophila and Lepidoptera species, largely refute a purely stochastic birth-death hypothesis (19,58,(63)(64)(65) . We found a similar pattern of fewer CYP450 gene numbers in S. flava , likely due to a narrowing of their dietary niche, coupled with high turnover rates (high gain + loss rate) and a modest, but biologically significant bloom in the canonical xenobiotic resistance gene Cyp6g1 .…”

Section: Gene Blooms Not Gene Family Expansions As a Consequence Ofmentioning

confidence: 99%

“…For example, the spider mite ( Tetranychus urticae ) and diamondback moth ( Plutella xylostella ) genomes harbor expanded gene families encoding enzymes involved in detoxification of plant secondary compounds (15)(16)(17) , and genes encoding gustatory receptors (GRs) involved in host finding have undergone extensive lineage-specific duplications in butterflies (18) . Although there are clear gene-family expansions arising from plant-insect interactions, including "blooms" of paralogs that emerge from single ancestral genes (13,19) , isolating herbivory as the causal agent of some of these exceptional genome-scale patterns remains controversial (20) . Herbivory evolved >25 million years ago in all of the eighteen arthropod lineages assayed using comparative genomics (Fig.…”

Section: Introductionmentioning

confidence: 99%

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Evolution of herbivory remodels aDrosophilagenome

Gloss

Dittrich

Lapoint

et al. 2019

Preprint

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SIGNIFICANCE STATEMENTThe origin of land plants >400 million years ago (mya) spurred the diversification of plant-feeding (herbivorous) insects and triggered an ongoing chemical co-evolutionary arms race. Because ancestors of most herbivorous insects first colonized plants >200 mya, the sands of time have buried evidence of how their genomes changed with their diet. We leveraged the serendipitous intersection of two genetic model systems: a close relative of yeast-feeding fruit fly ( Drosophila melanogaste r), the "wasabi fly" ( Scaptomyza flava ), that evolved to consume mustard plants including Arabidopsis thaliana . The yeast-to-mustard dietary transition remodeled the fly's gene repertoire for sensing and detoxifying chemicals. Although many genes were lost, some underwent duplications that encode the most efficient detoxifying enzymes against mustard oils known from animals. Gloss et al. 2019 1ABSTRACT One-quarter of extant Eukaryotic species are herbivorous insects, yet the genomic basis of this extraordinary adaptive radiation is unclear. Recently-derived herbivorous species hold promise for understanding how colonization of living plant tissues shaped the evolution of herbivore genomes. Here, we characterized exceptional patterns of evolution coupled with a recent (<15 mya) transition to herbivory of mustard plants (Brassicaceae, including Arabidopsis thaliana ) in the fly genus Scaptomyza, nested within the paraphyletic genus Drosophila . We discovered a radiation of mustard-specialized Scaptomyza species, comparable in diversity to the Drosophila melanogaster species subgroup. Stable isotope, behavioral, and viability assays revealed these flies are obligate herbivores. Genome sequencing of one species, S. flava, revealed that the evolution of herbivory drove a contraction in gene families involved in chemosensation and xenobiotic metabolism. Against this backdrop of losses, highly targeted gains ("blooms") were found in Phase I and Phase II detoxification gene sub-families, including glutathione S-transferase ( Gst ) and cytochrome P450 ( Cyp450 ) genes. S. flava has more validated paralogs of a single Cyp450 (N=6 for Cyp6g1 ) and Gst (N=5 for GstE5-8 ) than any other drosophilid. Functional studies of the Gst repertoire in S. flava showed that transcription of S. flava GstE5-8 paralogs was differentially regulated by dietary mustard oils, and of 22 heterologously expressed cytosolic S. flava GST enzymes, GSTE5-8 enzymes were exceptionally well-adapted to mustard oil detoxification in vitro . One, GSTE5-8a, was an order of magnitude more efficient at metabolizing mustard oils than GSTs from any other metazoan. The serendipitous intersection of two genetic model organisms, Drosophila and Arabidopsis , helped illuminate how an insect genome was remodeled during the evolutionary transformation to herbivory, identifying mechanisms that facilitated the evolution of the most diverse guild of animal life.

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“…35,36 This is supported by recent work demonstrating that similar molecular pathways (CYPQ9 enzyme family) are utilised by both honeybees and bumble bees in the detoxification of insecticides (e.g. pyrethroids, N-cyanoamidine neonicotinoids, organophosphorus compounds) and plant toxins such as flavonoids, [37][38][39] with solitary species (Osmia spp.) using analogues from a related CYP family (CYP9BU).…”

Section: Introductionmentioning

confidence: 88%

Are honeybees suitable surrogates for use in pesticide risk assessment for non‐Apisbees?

Thompson

Pamminger²

2019

Pest Management Science

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Historically, bee regulatory risk assessment for pesticides has centred on the European honeybee (Apis mellifera), primarily due to its availability and adaptability to laboratory conditions. Recently, there have been efforts to develop a battery of laboratory toxicity tests for a range of non‐Apis bee species to directly assess the risk to them. However, it is not clear whether the substantial investment associated with the development and implementation of such routine screening will actually improve the level of protection of non‐Apis bees. We argue, using published acute toxicity data from a range of bee species and standard regulatory exposure scenarios, that current first‐tier honeybee acute risk assessment schemes utilised by regulatory authorities are protective of other bee species and further tests should be conducted only in cases of concern. We propose similar analysis of alternative exposure scenarios (chronic and developmental) once reliable data for non‐Apis bees are available to expand our approach to these scenarios. In addition, we propose that in silico (simulation) approaches can then be used to address population‐level effects in more field‐realistic scenarios. Such an approach could lead to a protective, but also workable, risk assessment for non‐Apis species while contributing to pollination security in agricultural landscapes around the globe. © 2019 Society of Chemical Industry

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Genomic footprint of evolution of eusociality in bees: floral food use and CYPome “blooms”

Cited by 32 publications

References 41 publications

Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis

Genomic insights into neonicotinoid sensitivity in the solitary bee Osmia bicornis

Evolution of herbivory remodels aDrosophilagenome

Are honeybees suitable surrogates for use in pesticide risk assessment for non‐Apisbees?

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