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Influence of resistance traits on adult bee infestation/Coefficient of regression
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Ectoparasitic mite, Varroa destructor, today is one of the main reasons for colony losses worldwide. This study deals with relationships between measurements of resistance characteristics and measurements of bee infestation. During the trial, 105 Apis mellifera carnica colonies were tested according to AGT (Arbeitsgemeinschaft Toleranzzucht) breedi...
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To control Varroa destructor, an ectoparasitic mite, a honey bee line possessing high hygienic behavior (HHB) against this mite has been bred in South Korea. However, a method that can diagnose and assess the HHB line from control (the low hygienic behavior, LHB) line has not been reported yet. Thus, the objective of this study was to develop singl...
Citations
... These approaches include the selection of honey bees resistant to V. destructor (Harbo and Harris 1999, Büchler et al. 2010, Rinderer et al. 2010, Kefuss et al. 2016, Guichard et al. 2020a, that is, capable of keeping colony infestation at a bearable level, by means of defense mechanisms. Among the latter, suppressed mite reproduction (Harbo and Harris 2002, Buchegger et al. 2018, von Virag et al. 2022) and recapping of infested cells (Buchegger et al. 2018, Martin et al. 2019, Guichard et al. 2023 can decrease the quantity of mites which are born in the colony. Others, such as Varroa sensitive hygiene Harris 2009, Danka et al. 2016), where infested pupae are removed, and grooming , Morfin et al. 2020 can increase the number of mites which die. ...
... These approaches include the selection of honey bees resistant to V. destructor (Harbo and Harris 1999, Büchler et al. 2010, Rinderer et al. 2010, Kefuss et al. 2016, Guichard et al. 2020a, that is, capable of keeping colony infestation at a bearable level, by means of defense mechanisms. Among the latter, suppressed mite reproduction (Harbo and Harris 2002, Buchegger et al. 2018, von Virag et al. 2022) and recapping of infested cells (Buchegger et al. 2018, Martin et al. 2019, Guichard et al. 2023 can decrease the quantity of mites which are born in the colony. Others, such as Varroa sensitive hygiene Harris 2009, Danka et al. 2016), where infested pupae are removed, and grooming , Morfin et al. 2020 can increase the number of mites which die. ...
Since the global invasion of the ectoparasitic mite Varroa destructor (Anderson and Trueman), selection of mite-resistant honey bee (Apis mellifera L.) colonies appears challenging and has to date not broadly reduced colony mortality. The low published estimated heritability values for mite infestation levels could explain the limited genetic progresses obtained so far. We hypothesize that intercolonial horizontal mite transmission could differentially affect the single colonies located in a given apiary and therefore invisibly bias colony infestation phenotypes. This bias may be lower in regions with lower colony density, providing suitable conditions to set up evaluation apiaries. To verify these hypotheses, we monitored mite infestation and reinvasion in experimental colonies, as well as infestation in neighboring colonies belonging to beekeepers in three areas with variable colony densities in the canton of Bern, Switzerland during three consecutive beekeeping seasons. Mite immigration fluctuated between apiaries and years and significantly contributed to colony infestation level. Depending on apiary and year, 17–48% of the mites present in the experimental colonies at the time of the summer oxalic acid final treatment potentially derived from mite immigration that had occurred since mid-spring. Mite immigration was not linked to local colony density or the infestation levels of beekeepers’ colonies located within 2 km. Our results do not prove that apiaries for colony evaluation should necessarily be established in areas with low colony density. However, they highlight the high impact of beekeeping management practices on mite colony infestation levels.
... In the search for varroa resistance, many different traits linked to reduced mite viability have been examined. With regard to mite reproduction both, infertile and MNR (mite non-reproduction; infertile, no male, delayed development of offspring) are useful indicators that can help predict a colony's ability to withstand varroa infestation (Buchegger et al., 2018;Mondet et al., 2020). It is often hypothesized that high levels of infertile or MNR mites are due to the interruptive opening of brood cells by VSH bees, which forces the mother mites to invade a new cell after already commencing reproduction. ...
A sustainable solution to the global threat of the Varroa destructor mite is the selection of varroa‐resistant honey bee (Apis mellifera) colonies. Both “mite non‐reproduction” (MNR) and “varroa sensitive hygiene” (VSH) appear to be promising selection traits for achieving the goal of a resistant honey bee. MNR describes colonies that have a high number of non‐reproductive mites (no offspring, no males, or delayed development of mite offspring). High numbers of non‐reproductive mites have been observed in selected colonies, but the mechanism behind this trait has not yet been identified. The specialized hygienic behavior of selected honey bees, called VSH, is the removal of varroa‐infested brood. These traits were thought to be linked by VSH bees preferentially removing reproductive varroa females leaving only non‐reproductive mites behind in cells and thus creating colonies with high levels of MNR. To further investigate this link, we used an experimental setup and data sets from a four‐year selection project designed to breed for MNR and VSH colonies. In addition, we sought to answer the question of whether non‐reproductive mites are a direct consequence of worker removal behavior. To test this, we artificially induced removal behavior, and after providing the mite with enough time to re‐enter another cell, we opened all capped cells, relocated the mites, and evaluated their reproduction. As shown in previous studies and in this study, VSH had no effect on MNR levels. Also, the induced removal behavior did not lead to non‐reproduction in the subsequent reproductive cycle post interruption. We thus concluded that breeding for non‐reproductive mites does not automatically breed for VSH behavior and worker removal behavior does not cause subsequent reproductive failure of the mites forced to flee and find a new cell for reproduction.
... Although REC was frequently described as an important resistance trait 3,10,11,27 , beneficial effects for the host seem to be highly variable. At the colony level, high rates of REC were found to decrease Varroa reproduction in some cases 28,29 , while this could not be confirmed in others 17,23 . At the cell level, the results were likewise variable: effects on MNR were mainly shown for artificially uncapped cells 12 , while either no effect was found in naturally recapped cells 12,18,26 or results differed between sample sets 24 . ...
... Thus, it was proposed that the effect of REC may sometimes be overshadowed by other mechanisms 18,26 . This would also explain contradicting reports on the relationship between REC and infestation measures at the colony level 18,23,24,29,30 . Accordingly, we observed no correlation between RECinf and infestation measures or RECinf and MNR at the colony level (Table 3), although MNR was increased in the case of REC at the cell level (Fig. 1a, Table 1). ...
Resistance traits of honeybees (Apis mellifera) against their major parasite Varroa destructor have fascinated scientists and breeders for long. Nevertheless, the mechanisms underlying resistance are still largely unknown. The same applies to possible interactions between host behaviours, mite reproduction and seasonal differences. Two resistance traits, reproductive failure of mites and recapping of brood cells, are of particular interest. High rates of recapping at the colony level were found to correspond with low reproductive success of mites. However, the direct effect of recapping on mite reproduction is still controversial and both traits seem to be very variable in their expression. Thus, a deeper knowledge of both, the effect of recapping on mite reproduction and the seasonal differences in the expression of these traits is urgently needed. To shed light on this host-parasite interaction, we investigated recapping and mite reproduction in full-grown colonies naturally infested with V. destructor. Measurements were repeated five times per year over the course of 3 years. The reproductive success of mites as well as the recapping frequency clearly followed seasonal patterns. Thereby, reproductive failure of mites at the cell level was constantly increased in case of recapping. Interestingly, this did not apply to the occurrence of infertile mites. In line with this, recapping activity in fertile cells was most frequent in brood ages in which mite offspring would be expected. Our results suggest that mite offspring is the main target of recapping. This, in turn, leads to a significantly reduced reproductive success of the parasite.
... A recapping test was developed because the natural survival of multiple resistant honey bee populations is associated with a high recapping rate [13,15], suggesting its role in promoting colony resistance. However, the current protocols for evaluating recapping rates are very time consuming, as this process includes the opening of hundreds of individual cells [13,16]. To increase the applicability of this trait, we developed a simplified protocol ('Recapping') which allows for a cost-and time-effective evaluation of this trait. ...
For the development of novel selection traits in honey bees, applicability under field conditions is crucial. We thus evaluated two novel traits intended to provide resistance against the ectoparasitic mite Varroa destructor and to allow for their straightforward implementation in honey bee selection. These traits are new field estimates of already-described colony traits: brood recapping rate (‘Recapping’) and solidness (‘Solidness’). ‘Recapping’ refers to a specific worker characteristic wherein they reseal a capped and partly opened cell containing a pupa, whilst ‘Solidness’ assesses the percentage of capped brood in a predefined area. According to the literature and beekeepers’ experiences, a higher recapping rate and higher solidness could be related to resistance to V. destructor. During a four-year field trial in Switzerland, the two resistance traits were assessed in a total of 121 colonies of Apis mellifera mellifera. We estimated the repeatability and the heritability of the two traits and determined their phenotypic correlations with commonly applied selection traits, including other putative resistance traits. Both traits showed low repeatability between different measurements within each year. ‘Recapping’ had a low heritability (h2 = 0.04 to 0.05, depending on the selected model) and a negative phenotypic correlation to non-removal of pin-killed brood (r = −0.23). The heritability of ‘Solidness’ was moderate (h2 = 0.24 to 0.25) and did not significantly correlate with resistance traits. The two traits did not show an association with V. destructor infestation levels. Further research is needed to confirm the results, as only a small number of colonies was evaluated.
... A less-costly mechanism is the uncapping-recapping behavior, which is more likely to be favored by natural selection, as it reduces mortality of the bee pupae and increases colony competitiveness. Such uncapping of sealed brood cells without removal of the pupae, followed by their recapping, is common in all honey bee populations [46,119,[125][126][127][128] and is of low cost for the colony since no brood is sacrificed in the action. Association between recapping and reduced mite reproductive success has been reported from a population bred for VSH [129] and also from four naturally V. destructor-surviving populations in Europe [61,63,128], in Brazil and South Africa, [127] and in A. m. scutellata as well [46]. ...
... Such uncapping of sealed brood cells without removal of the pupae, followed by their recapping, is common in all honey bee populations [46,119,[125][126][127][128] and is of low cost for the colony since no brood is sacrificed in the action. Association between recapping and reduced mite reproductive success has been reported from a population bred for VSH [129] and also from four naturally V. destructor-surviving populations in Europe [61,63,128], in Brazil and South Africa, [127] and in A. m. scutellata as well [46]. ...
Developing resistance to the varroa mite in honey bees is a major goal for apicultural science and practice, the development of selection strategies and the availability of resistant stock. Here we present an extended literature review and survey of resistant populations and selection programs in the EU and elsewhere, including expert interviews. We illustrate the practical experiences of scientists, beekeepers, and breeders in search of resistant bees. We describe numerous resistant populations surviving without acaricide treatments, most of which developed under natural infestation pressure. Their common characteristics: reduced brood development; limited mite population growth; and low mite reproduction, may cause conflict with the interests of commercial beekeeping. Since environmental factors affect varroa mite resistance, particular honey bee strains must be evaluated under different local conditions and colony management. The resistance traits of grooming, hygienic behavior and mite reproduction, together with simple testing of mite population development and colony survival, are significant in recent selection programs. Advanced breeding techniques and genetic and physiological selection tools will be essential in the future. Despite huge demand, there is no well-established market for resistant stock in Europe. Moreover, reliable experience or experimental evidence regarding the resistance of stocks under different environmental and management conditions is still lacking.
... VSH is also triggered in response to brood characteristics, specifically odor cues emitted by infested pupae [92][93][94][95] and, possibly, by V. destructor [96]. The uncapping-recapping behavior has recently gained attention as a target for selection towards resistance [72,73,97]. However, a lack of knowledge about how the factors influence its expression currently limits its use as target trait. ...
... Table S4. Link between 'uncapping-recapping' and colony survival or infestation level reported in literature [73,97,117,306]. Table S5. ...
... Table S5. Link between 'hygienic behaviour towards dead brood' and colony survival or infestation level reported in literature [42,97,172,183,185,215,231,270,312,315,319,320,324,325,327,328,340,[349][350][351][352][353][354][355][356][357][358][359][360][361][362][363][364][365][366]. Table S6. ...
Background
In spite of the implementation of control strategies in honey bee ( Apis mellifera ) keeping, the invasive parasitic mite Varroa destructor remains one of the main causes of colony losses in numerous countries. Therefore, this parasite represents a serious threat to beekeeping and agro-ecosystems that benefit from the pollination services provided by honey bees. To maintain their stocks, beekeepers have to treat their colonies with acaricides every year. Selecting lineages that are resistant to infestations is deemed to be a more sustainable approach.
Review
Over the last three decades, numerous selection programs have been initiated to improve the host–parasite relationship and to support honey bee survival in the presence of the parasite without the need for acaricide treatments. Although resistance traits have been included in the selection strategy of honey bees, it has not been possible to globally solve the V. destructor problem. In this study, we review the literature on the reasons that have potentially limited the success of such selection programs. We compile the available information to assess the relevance of selected traits and the potential environmental effects that distort trait expression and colony survival. Limitations to the implementation of these traits in the field are also discussed.
Conclusions
Improving our knowledge of the mechanisms underlying resistance to V. destructor to increase trait relevance, optimizing selection programs to reduce environmental effects, and communicating selection outcomes are all crucial to efforts aiming at establishing a balanced relationship between the invasive parasite and its new host.
... Recapping, a less costly option for the bees, is expressed by the uncapping of the infested brood by the nurse bees, followed by a subsequent recapping of the cell without harming the developing pupae [29][30][31]. So far, the outcome of selecting MNR colonies ranges from successfully identifying and selecting MNR colonies [12,[32][33][34] to seeing no effect on the survival of honey bee colonies when looking at their MNR trait [35][36][37][38]. While it is possible to pin this on differences in the survival mechanisms used by distinct honey bee populations [12], it is also possible that this is at least partially due to methodological biases. ...
In the current context of worldwide honey bee colony losses, among which the varroa mite plays a major role, the hope to improve honey bee health lies in part in the breeding of varroa resistant colonies. To do so, methods used to evaluate varroa resistance need better understanding. Repeatability and correlations between traits such as mite non-reproduction (MNR), varroa sensitive hygiene (VSH), and hygienic behavior are poorly known, due to practical limitations and to their underlying complexity. We investigate (i) the variability, (ii) the repeatability of the MNR score, and (iii) its correlation with other resistance traits. To reduce the inherent variability of MNR scores, we propose to apply an empirical Bayes correction. In the short-term (ten days), MNR had a modest repeatability of 0.4, whereas in the long-term (a month), it had a low repeatability of 0.2, similar to other resistance traits. Within our dataset, there was no correlation between MNR and VSH. Although MNR is amongst the most popular varroa resistance estimates in field studies, its underlying complex mechanism is not fully understood. Its lack of correlation with better described resistance traits and low repeatability suggest that MNR needs to be interpreted cautiously, especially when used for selection.
... Recapping, a less costly option for the bees, is expressed by the uncapping of the infested brood by the nurse bees, followed by a subsequent recapping of the cell without harming the developing pupae [29][30][31]. So far, the outcome of selecting MNR colonies ranges from successfully identifying and selecting MNR colonies [12,[32][33][34] to seeing no effect on the survival of honey bee colonies when looking at their MNR trait [35][36][37][38]. While it is possible to pin this on differences in the survival mechanisms used by distinct honey bee populations [12], it is also possible that this is at least partially due to methodological biases. ...
In the current context of worldwide honey bee colony losses, among which the varroa mite plays a major role, hope to improve honey bee health lies in part in the breeding of varroa resistant colonies. To do so, methods used to evaluate varroa resistance need better understanding. Repeatability and correlations between traits such as Mite Non-Reproduction (MNR), Varroa Sensitive Hygiene (VSH) and hygienic behaviour are poorly known, due to practical limitations and to their underlying complexity. We investigate (i) the variability, (ii) repeatability of the MNR score and (iii) its correlation with other resistance traits. To reduce the inherent variability of MNR scores, we propose to apply an Empirical Bayes correction. On the short-term (ten days) MNR had a modest repeatability of 0.4 whereas on the long- term (a month) it had a low repeatability of 0.2, similar to other resistance traits. Within our dataset there was no correlation between MNR and VSH. Although MNR is amongst the most popular varroa resistance estimates in field studies, its underlying complex mechanism is not fully understood. Its lack of correlation with better described resistance traits and low repeatability suggest that MNR need to be interpreted cautiously, especially when used for selection.
... This large-scale colony loss has led to decreased availability of hive products like honey and pollination services (Aizen and Harder 2009;Potts et al. 2010;Flottum 2018). One of the key contributors to this decline has been the infestation of hives with the Varroa destructor mite (Buchegger et al. 2018). To combat V. destructor, the synthetic pyrethroid tau-fluvalinate, hereafter referred to as fluvalinate, has been heavily used by beekeepers. ...
Fluvalinate has been extensively used in the United States to combat honey bee colony loss due to Varroa destructor mites. The objectives of the current research project were to investigate the extent of fluvalinate contamination in commercially available wax and to define exposure pathways to larval and adult honey bees. All of the commercial wax tested contained elevated fluvalinate concentrations, indicating a need for regulation of the sources of wax being rendered for resale. Based on the negative logarithm of the partition coefficient between wax and pollen (‐0.54), it is evident that fluvalinate has the potential to actively transfer from the contaminated wax into hive matrices. This was confirmed by adding fluvalinate‐dosed wax, fluvalinate‐impregnated strips, or a combination of the two to hives. Larvae and adult bees were checked for fluvalinate exposure using gas chromatography‐mass spectrometry analysis. Larvae had detectable concentrations of fluvalinate in all treatments. Bioaccumulation in adult bees was significantly affected by the interaction between treatment type and application time. In other words, residues were comparable from hives that only had fluvalinate‐dosed wax to those that were actively being treated, suggesting that transfer of fluvalinate from wax into adult bees was an important exposure route. In conclusion, exposure of fluvalinate from contaminated wax and treatment strips to honey bees needs to be considered when evaluating risk for colony loss in hives. This article is protected by copyright. All rights reserved.
Several resistance traits have been proposed to select honey bees (Apis mellifera L.) that can survive in the presence of parasitic mite Varroa destructor (Anderson and Trueman) and enable a more sustainable apiculture. The interest for uncapping-recapping has recently increased following its identification in several naturally surviving honey bee populations, yet the utility of this trait for human-mediated selection is poorly known. Here, we evaluated the repeatability of recapping and its correlations with mite infestation levels, and assessed the expression of the trait in the often neglected drone brood. We also calculated correlations between recapping, mite infertility, and mite fecundity, expressed either at the level of individual brood cells or of the whole colony. Recapping measured in worker brood showed moderate repeatability (ranging between 0.30 and 0.46). Depending on sample, recapping slightly correlated negatively with colony infestation values. Recapping was also measured in drone brood, with values often comparable to recapping in worker brood, but no significant correlations were obtained between castes. At cell level, recapped cells in drone brood (but not in workers) were significantly less infested than nonrecapped cells, whereas in workers (but not in drones), recapped cells hosted mites with significantly lower fecundity. At colony level, with a few exceptions, recapping did not significantly correlate with mite infertility and fecundity, caste, sample, or number of infested cells considered. These results indicate limited possibilities of impeding mite reproduction and possibly mite infestation of honey bee colonies by recapping, which would need to be confirmed on larger, different populations.
