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Seasonal trade-offs shape metabolomic and proteomic responses to Varroa destructor parasitisation in honey bees

ABSTRACT: The ectoparasitic mite Varroa destructor is a major driver of honey bee mortality, yet its impact depends on the specific phenotypes of summer and winter worker bees. Here, we apply an LC-MS/MS-based proteomics to dissect how Varroa parasitisation affects the molecular physiology of short-lived summer and long-lived winter worker bees. Newly generated proteomic data from summer bees were integrated with a previously published winter bees dataset (PXD030369), enabling direct seasonal comparison under identical analytical pipelines. Heads and abdomens from two experimental groups (varroa parasitised labelled as “Varroa”, healthy control labelled as “Unpara”) and two seasonal phenotypes (summer and winter) were compared. Despite strong seasonal divergence, a conserved Varroa-associated proteomic changes emerged across seasons, characterised by enhanced cellular logistics and membrane remodelling coupled with compromised metabolic robustness and nutritional output. Together, our results demonstrate that V. destructor does not elicit a uniform stress response but exploits seasonally distinct physiological states of honey bees, generating divergent molecular stress patterns with direct implications for worker survival and colony resilience.

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ORGANISM(S): Apis Mellifera (honeybee)

TISSUE(S): Head, Abdomen

SUBMITTER: Jacek Marciniak

LAB HEAD: Pavel Dobes

PROVIDER: PXD073444 | Pride | 2026-03-11

REPOSITORIES: Pride

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Project description:As a matter of fact, honeybees are vital for the pollination of more than 80 crops of agricultural interest. However, population decline has become an important global issue causing significant concerns among agricultural experts and the broader public. For this, parasites are known to be the major culprits responsible for the losses of millions of honeybee colonies so far. Among these parasites, Varroa destructor has been identified as a major cause for global losses in Western honeybee (Apis mellifera) colonies. Hygienic behavior (HB), on the other hand, is a collective response by adult honeybees to defend against parasites and diseases that is known to involve in resistance towards Varroosis. Even with the efforts made to elucidate the molecular mechanism underlying HB, it is still not understood. In our study, we have studied the proteomic correlates to HB using a honeybee line (selected for Varroa-specific HB for over a decade in Germany). We sampled individual worker bees from this line that showed HB after closer infrared video observations and compared the proteomes of their mushroom bodies and antennae with those of workers that came from the same set of colonies but didn't show the behaviour. Furthermore, we compared the pupal hemolymph for worker bees of the selected HB line and a control line using state-of-the art techniques of proteomics. We identified a total of 8609 proteins (covered >55% of the honeybee proteome) from these three honeybee tissues. This is the most comprehensive proteomic study of the honeybee HB to date, and the first to focus on individual bees expressing Varroa-specific HB. These results have significantly advanced our knowledge on the biology underlining HB to a new level. The uniquely found functional classes and pathways by the proteins identified in each tissue suggest that hygienic bees have shaped distinct proteome settings to underpin the HB. Moreover, during analysis of pupal hemolymph proteome, the HB-line has adapted a unique strategy to boost an individual and social immunity and drove pupal organogenesis via energy metabolism and protein biosynthesis. Moreover, in the mushroom bodies of different HB phenotypic worker bees, the hygienic bees have enhanced their neuronal sensitivity to promote the execution of HB by activation of synaptic vesicles and calcium channel activities. Moreover, in the antennae of two HB phenotypic worker bees, the hygienic bees have demonstrated strengthening of their sensitivity associated with olfactory senses and signal transmissions, which is important to input a strong signal to the mushroom bodies and initiate HB. In conclusion, our novel findings have significantly extended our understandings of the molecular mechanisms that underline the HB to combat Varroa infestation. Furthermore, we identified a wide array of novel markers that are useful for accelerating marker associated selection of HB to aid in the natural resistance to a parasite blamed for a global decline in honeybee health.

			Action	DRS
	PXD073444.sdrf.tsv	Tabular
	checksum.txt	Txt
	mzTab_abdomens.mzTab	Mztab
	mzTab_heads.mzTab	Mztab
	proteinGroups_abdomens.txt	Txt

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Seasonal trade-offs shape metabolomic and proteomic responses to Varroa destructor parasitisation in honey bees

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