The rise and fall of major royal jelly proteins during a honeybee (<i>Apis mellifera</i>) workers' life

Dobritzsch, Dirk; Aumer, Denise; Fuszard, Matthew; Erler, Silvio; Buttstedt, Anja

doi:10.1002/ece3.5429

Cited by 33 publications

(40 citation statements)

References 64 publications

(129 reference statements)

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“…MRJP seems to have evolved recently deriving from the Yellow family of genes and it seems to have diversified independently in each species where it has been found. In honeybees, MRJP is mostly expressed in workers (particularly nurses) but also other castes 56,57 , and besides being involved in the production of Royal Jelly, it has also been associated with brain function 58 , caste determination and many aspects of eusociality 54 . These functions seem to derive from Royal Jelly's function in establishing division of labour in the colonies through determining the development of larvae into queens and worker.…”

Section: Discussionmentioning

confidence: 99%

Declining genetic diversity of European honeybees along the twentieth century

Themudo

Rey‐Iglesia

Tascón

et al. 2020

Sci Rep

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the european honeybee (Apis mellifera) is a key pollinator and has in the last decades suffered significant population decline. A combination of factors, including decrease in genetic diversity and introduction of Varroa mites, have been suggested to be responsible for these losses, but no definitive cause has yet been appointed. In Europe not only have wild colonies been severely affected, but managed hives have had a massive decline in numbers. To test the hypothesis that honeybees' genetic diversity has decreased in the recent past, we used reduced representation genome sequencing of 40 historical honeybee specimens collected in natural History collections across europe and compared them to genomic data from 40 individuals from extant populations (collected post 2006). Our results are consistent with the existence of five evolutionary lineages as previously described, and show a decrease in genetic diversity between historical and extant individuals of the same lineage, as well as high levels of admixture in historical specimens. Our data confirm that a loss of genetic diversity has occurred during the last century, potentially increasing honeybees' vulnerability to contemporary ecological and anthropogenic stressors. Honeybees are one of the most important pollinator species and the most widely used insect, managed for its pollination services and production of honey. The number of managed honeybee colonies in Europe has generally decreased since the 1960′s, at least in Central Europe 1. The number of wild or feral honey bees is less known, with many believing or assuming that they no longer exist. Recent work however suggests that feral honey bees still colonize beech forests in Germany, and probably much of Central Europe 2. Even though bees have been used to produce honey and for pollination purposes for over 7,000 years, since at least Ancient Egypt civilizations 3-5 , it was only when beekeeping techniques were perfected in the seventeenth and eighteenth centuries that it became possible to maintain large bee colonies giving rise to modern apiculture 6. More recent practices, such as the commercial mass rearing of queens, artificial selection of behaviours favouring honey production, and the presence of thousands of bees in limited spaces, may have altered the natural processes and affected the genetic diversity of domestic and wild (or feral) hives, increasing their susceptibility and the transmission rate of diseases between bees 7. There is an ongoing debate about whether European honeybees are domesticated (in the sense that selective breeding over generations has led to artificial selection) or not 8-10. Traits favourable to beekeepers, such as docility, lack of propensity to swarming, honey yield, and others may be selected for, but as it is difficult to have controlled mating, this is usually done through the import of stock from other areas, where these traits are more frequent. This has consequences for wild populations, as due to the wide freedom honeybees have even when in artificial hives 9 ,...

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Section: Discussionmentioning

confidence: 99%

Declining genetic diversity of European honeybees along the twentieth century

Themudo

Rey‐Iglesia

Tascón

et al. 2020

Sci Rep

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“…The majority of all honey proteins were MRJP 1, 2 and 3, with MRJP1 being the most abundant and MRJP2 and 3 being detected in equal concentrations (Table 1). In spite of the very high similarity of MRJPs [31], a distinct identification of MRJP 5 and 7 was possible, using the modified reference honey bee protein data base [30] that excluded similar peptides of highly related proteins. The molecular weight (MW) of all identified proteins matched well with the protein bands shown in Figure 2 (MW values see Table 1).…”

Section: Resultsmentioning

confidence: 99%

“…Furthermore, we were unable to detect apisimin (~8 kDa) and defensin-1 (~11 kDa). This is unsurprising, as apisimin generates only one possible tryptic peptide which may not ‘fly’ in mass spectrometric analyses [30], and defensin-1 is mostly present in honey with <1% of the total honey proteome [38], which might explain its absence in our samples. Nevertheless, in Figure 2, a single band (evenly present in all samples) slightly above 10 kDa can be observed, which might be defensin-1 (10.717 kDa).…”

Section: Discussionmentioning

confidence: 99%

“…Full searches were run through Byonic v3.3.11 (Protein Metrics, Cupertino, CA, USA) with the additional following settings: the maximum number of precursors per MS2 was set to 10, as recommended by the manufacturer for MSE data. Protein FDR was set to 1%, against both A. mellifera (Amel_4.5) and an internally curated focused database generated for A. mellifera hypopharyngeal glands and brains, consisting of sequences emphasised for uniqueness (database curation procedure published earlier [30]). Output mzIdentML files were then loaded into Scaffold Q + S 4.8.9 (Proteome Software Inc., Portland, OR, USA).…”

Section: Methodsmentioning

confidence: 99%

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The Effect of Diet on the Composition and Stability of Proteins Secreted by Honey Bees in Honey

Lewkowski

Mureșan

Dobritzsch

et al. 2019

Insects

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Honey proteins are essential bee nutrients and antimicrobials that protect honey from microbial spoilage. The majority of the honey proteome includes bee-secreted peptides and proteins, produced in specialised glands; however, bees need to forage actively for nitrogen sources and other basic elements of protein synthesis. Nectar and pollen of different origins can vary significantly in their nutritional composition and other compounds such as plant secondary metabolites. Worker bees producing and ripening honey from nectar might therefore need to adjust protein secretions depending on the quality and specific contents of the starting material. Here, we assessed the impact of different food sources (sugar solutions with different additives) on honey proteome composition and stability, using controlled cage experiments. Honey-like products generated from sugar solution with or without additional protein, or plant secondary metabolites, differed neither in protein quality nor in protein quantity among samples. Storage for 4 weeks prevented protein degradation in most cases, without differences between food sources. The honey-like product proteome included several major royal jelly proteins, alpha-glucosidase and glucose oxidase. As none of the feeding regimes resulted in different protein profiles, we can conclude that worker bees may secrete a constant amount of each bee-specific protein into honey to preserve this highly valuable hive product.

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“…The top differentially expressed genes between males and females for each tissue appear to be related to the sex-specific tasks of the adults (Supplemental Table 5). For example, females, which must properly provision their eggs, had elevated expression for a vitellogenin-like gene, which is associated with egg yolk formation, hormone regulation, lifespan, and foraging behavior (Ihle, Page, Frederick, Fondrk, & Amdam, 2010; Munch, Ihle, Salmela, & Amdam, 2015; Nunes, Ihle, Mutti, Simoes, & Amdam, 2013; Seehuus, Norberg, Gimsa, Krekling, & Amdam, 2006; Wheeler, Ament, Rodriguez-Zas, & Robinson, 2013) There was also increased expression for many major royal jelly protein family genes, known to play a role reproductive maturation and tending to young (Buttstedt, Moritz, & Erler, 2013; Dobritzsch, Aumer, Fuszard, Erler, & Buttstedt, 2019; Drapeau, Albert, Kucharski, Prusko, & Maleszka, 2006). Among the genes with unusually high expression in males were three chemosensory genes (OR54, OR22, and OBP9) that were particularly high in the antennae and may play a role in mate finding.…”

Section: Resultsmentioning

confidence: 99%

Support for the Adaptive Decoupling Hypothesis from Whole-Transcriptome Profiles of a Hypermetamorphic and Sexually Dimorphic Insect,Neodiprion lecontei

Herrig

Vertacnik

Kohrs

et al. 2019

Preprint

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Complex life cycles-especially those with distinct larval and adult stages separated by a complete metamorphic event-are common in animals. The adaptive decoupling hypothesis (ADH) proposes that metamorphosis is an adaptation for optimizing expression of traits across life stages that experience opposing selection pressures. Similarly, sex-biased expression of traits is thought to evolve in response to sexually antagonistic selection. Both hypotheses predict that traits will be decoupled (i.e., genetically uncorrelated) among developmental stages and sexes, but direct comparisons between stage-specific and sex-specific decoupling are rare. Additionally, tests of the ADH have been hampered by a lack of suitable traits for among-stage comparisons and by uncertainties regarding how much decoupling is to be expected. To fill these voids, we characterize transcriptome-wide patterns of gene-expression decoupling in the hypermetamorphic and sexually dimorphic insect, Neodiprion lecontei. This species has three ecologically and morphologically distinct larval stages separated by molts, as well as a complete metamorphic transition that produces dimorphic adult males and females. Consistent with the ADH, we observe that: (1) the decoupling of gene expression becomes more pronounced as the ecological demands of developmental stages become more dissimilar and (2) gene-expression traits that mediate changing ecological interactions show stronger and more variable decoupling than expression traits that are likely to experience more uniform selection. We also find that gene-expression decoupling is more pronounced among major life stages than between the sexes. Overall, our results demonstrate that patterns of gene-expression decoupling can be predicted based on gene function and organismal ecology. Significance Statement8 out of 10 animals undergo a metamorphic transition at some point in their life. The adaptive decoupling hypothesis proposes that metamorphosis is widespread because it enables natural selection to act independently on traits expressed at different stages. Using four ecologically distinct life stages of the redheaded pine sawfly, we show that the dissimilarity of gene expression profiles can be predicted based on the ecological dissimilarity of the life stages and on whether these genes impact ecological interactions. We also find that gene expression is more dissimilar between drastic life stages than between different sexes. Together, these results provide strong support for a core assumption of the ADH: that metamorphosis enables organisms to optimize genetic correlations across development.

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The rise and fall of major royal jelly proteins during a honeybee (Apis mellifera) workers' life

Cited by 33 publications

References 64 publications

Declining genetic diversity of European honeybees along the twentieth century

Declining genetic diversity of European honeybees along the twentieth century

The Effect of Diet on the Composition and Stability of Proteins Secreted by Honey Bees in Honey

Support for the Adaptive Decoupling Hypothesis from Whole-Transcriptome Profiles of a Hypermetamorphic and Sexually Dimorphic Insect,Neodiprion lecontei

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