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Correlations between repeated measurements of BINF (1-3), above the diagonal and standard errors below the diagonal.
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Infestation with the parasitic mite Varroa destructor is a serious cause of bee colony (Apis mellifera) losses on a global level. However, the presence of untreated survivor populations in many different regions indicates that selection for resistance might lead to a long-term solution. The success of selection depends on suitable testing criteria....
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... r is the Pearson correlation between two traits and N is the number of cases where both traits were recorded. For a table with correlations between all pairs of traits with standard errors see Supplementary Table S3. This supplementary table also contains the 90% and 99% confidence intervals. ...Context 2
... Table 3 for these correlations for BINF (data for BINF 4-5 are included in Supplementary Table S3). In the dataset from Germany, the correlations were in the order of magnitude of 0.55, but in the Croatian data, they were significantly higher. ...Context 3
... Table 3 for these correlations for BINF (data for BINF 4-5 are included in Supplementary Table S3). In the dataset from Germany, the correlations were in the order of magnitude of 0.55, but in the Croatian data, they were significantly higher. ...Context 4
... significant effect of the infestation level on invasion rate of mites might also explain why we found a negative correlation of BINFa and b3 on the untreated and more highly infested colonies in Germany, while there is a positive correlation measured in the lower infested test populations in Austria and Croatia (Supplementary Table S3). ...Context 5
... differences in mite reproduction (SMR) are negatively correlated with brood infestation (BRINF) and mite population increase (b3), a repeatability of measurements close to zero indicates that its application might not be efficient for selective breeding programs. Table-S2-test-of-fixed-effects.pdf: adjustment of observations; Table-S3-correlations-200823.xlxs: Table with all correlations, confidence intervals and standard ...Similar publications
Cuban beekeeping has developed through a series of selection programs to its current state, characterized by the absence of chemical treatments for honey bee diseases. In 2013, the Cuban Bee Selection, Improvement and Breeding Program was launched to further optimize honey bee colonies. In this study, we analyzed the performance of the initial six...
Infestation with Varroa destructor is a serious cause of bee colony (Apis mellifera) losses on a global level. However, the presence of untreated survivor populations in many different regions supports the idea that selection for resistance can be successful. As colony survival is difficult or impossible to measure, differences in mite infestation...
Citations
... The detrimental effects of V. destructor and the impacts of acaricides on honeybee colonies have prompted beekeepers to seek sustainable approaches to control the mite. In order to achieve this, some beekeepers are trying to breed resistant honeybee stocks against V. destructor by using different selection criteria [5][6][7]. The social behavior of honeybees has called on the attention of beekeepers to address their intra-specific and inter-specific relationships while placing emphasis on their intrinsic behavior to reduce the spread of V. destructor. ...
... In a more recent study, the same researchers documented that the proportion of non-reproducing mites was positively correlated with the expression of VSH [63,69]. As the importance of hygienic behavior and its heritability became known, selective breeding of honeybee colonies against V. destructor gained value [5,7,102,103]. The sensitivity of honeybees to this behavior could be improved through field tests with compounds related to larval signaling [104]. ...
The ectoparasitic mite Varroa destructor is well known for transmitting a number of viruses that can contribute to the collapse of honeybee colonies. To date, the many control measures put in place to limit the spread of V. destructor have yielded no satisfactory results. This is challenging because the effect of the parasite on honeybee colonies is becoming notorious. This has weakened the beekeeping industry and reduced pollination services, which may contribute to global food insecurity in the future. Therefore, it is necessary to put in place possible control measures and outline sustainable approaches to mitigate research efforts against the Varroa destructor. Extensive research to elaborate on the best possible solution has revealed that the selective breeding of naturally occurring V. destructor immune-related traits of honeybee strains is sustainable. Since the Integrated Pest Management approach was introduced, while still being very unreliable, there are open questions as to what control strategy could be considered effective. After cross-examination of existing strategies, a more practical way could be the adoption of an integrated approach. This approach should involve the association of selective breeding of honeybee colonies with V. destructor immune-related traits and the application of soft chemical treatment.
... Varroa mite control strategies generate additional expenses for beekeepers, such as the cost of medications and additional workload. There is thus keen interest in selecting and breeding bees for Varroa resistance and tolerance (Kirrane et al. 2014;Uzunov et al. 2014;Danka et al. 2016;Büchler et al. 2020). In recent decades, natural populations of Varroa-resistant bees have been found (Fries et al. 2006;Locke et al. 2012), but most of these colonies lack the desired traits for beekeeping and pollination (Guichard et al. 2023). ...
... However, with the extremely high variability, we currently see that in daughter colonies, every subsequent generation requires a costly and time-consuming evaluation of the MNR and VSH traits in every colony to determine the individual daughters that express high levels of the desired traits. This high variance in offspring values puts into question the currently common strategy of selective breeding for Varroa resistance (Büchler et al. 2010(Büchler et al. , 2020. Simply breeding from the highest performers and expecting similar resistance in all the daughter colonies is clearly a faulty notion. ...
The honey bee ectoparasite Varroa destructor is the main cause of honey bee colony losses worldwide. Over the last decades, several projects have focused on improving the robustness of Apis mellifera against this parasitic mite. Selection traits, such as mite non-reproduction (MNR) and Varroa sensitive hygiene (VSH), are favored selection factors in Varroa resistance projects. VSH is a trait where adult honey bees remove the Varroa -infested brood. During this process, the female mites are arrested in their reproductive cycle leading to a reduction of the Varroa population within the bee colony. From 2019 to 2022, 1402 queens were instrumentally inseminated with single or multiple drones in a breeding program. Colonies headed by these queens were established annually, and the MNR and VSH levels were analyzed. VSH was evaluated in response to cells artificially infested with Varroa , and colonies with high VSH values were used to generate our selected VSH stock. Despite crossing high VSH drones and queens, we measured a remarkable heterogeneity of MNR and VSH in the next generation(s), most likely due to the well-described, high recombination rate in the honey bee genome. When assessed multiple times in the same colony, great variance between measurements was observed. Detailed evaluations of daughter colonies are thus required if selection programs want to breed colonies with reliable VSH traits. This constant need to evaluate all offspring to ensure the desirable resistance traits are present results in high workloads and great expenses in selection programs. Furthermore, such large-scale breeding programs are inefficient due to high fluctuations between measurements and generations, indicating we need to develop new approaches and improved methods for assessing Varroa resistance.
... In farm animals, resilience is defined as the capacity of animals (here colonies) to remain productive when exposed to environmental or infectious challenges (Colditz and Hine 2016). Part of the effort to improve resilience is linked to disease resistance, including via the control of the parasitic V. destructor mite (Rinderer et al. 2010;Danka et al. 2016;Büchler et al. 2020;Guichard et al. 2020a). Furthermore, there is also a growing interest in enhancing feed autonomy of colonies when facing fluctuating feed resources, as feed shortages are common in a wide range of landscapes (e.g., Czekońska et al. 2023). ...
There is growing interest in selective breeding of the honeybee, resulting in the emergence of new breeding projects, often with an emphasis on improving resilience traits, in particular toward brood diseases. Lately, feed autonomy is also gaining importance. Here, we use data from a small breeding nucleus in France to estimate genetic parameters for common bee breeding traits and a novel trait reflecting honey reserves in the brood chamber. Open-mated queens were produced each year from inseminated dams between 2019 and 2021, and ~330 colonies were phenotyped each following year at three periods during the entire beekeeping season. Genetic parameters were estimated using ReML with an animal model. Narrow-sense heritability estimates ranged from low (around 0.15) for calmness and total capped brood surface both measured in early summer, to moderate (0.30 to 0.40) for hygienic behavior in spring, honey yield, and phoretic V. destructor load in early summer. Honey reserves in the brood chamber showed an intermediate heritability throughout the season (around 0.25). Gentleness had a null heritability. Most correlations between phenotypes adjusted for environmental fixed effects were close to zero. Among exceptions, there were honey reserves in the brood chamber in early summer with honey yield (around −0.2) and with the total capped brood surface in early summer (around −0.3). These estimates, although uncertain due to the dataset size, suggest that selection for production and resilience will be effective, even though simultaneous selection for honey yield and feed reserves might be difficult due to a possible genetic antagonism between both traits.
... The goal of sustainable beekeeping is the long-term maintenance of honey bee colonies with respect to their natural behavior and local adaptation. One sustainable way of applying varroa mite control is through the selective breeding of colonies expressing naturally occurring, heritable mite resistance traits [20][21][22][23]. For example, Varroa Sensitive Hygiene, the detection and removal of varroa-infested brood, mainly explained mite resistance in naturally surviving colonies from Avignon, France [21,24]. ...
Implementation of marker-assisted selection (MAS) in modern beekeeping would improve sustainability, especially in breeding programs aiming for resilience against the parasitic mite Varroa destructor. Selecting honey bee colonies for natural resistance traits, such as brood-intrinsic suppression of varroa mite reproduction, reduces the use of chemical acaricides while respecting local adaptation. In 2019, eight genomic variants associated with varroa non-reproduction in drone brood were discovered in a single colony from the Amsterdam Water Dune population in the Netherlands. Recently, a new study tested the applicability of these eight genetic variants for the same phenotype on a population-wide scale in Flanders, Belgium. As the properties of some variants varied between the two studies, one hypothesized that the difference in genetic ancestry of the sampled colonies may underly these contribution shifts. In order to frame this, we determined the allele frequencies of the eight genetic variants in more than 360 Apis mellifera colonies across the European continent and found that variant type allele frequencies of these variants are primarily related to the A. mellifera subspecies or phylogenetic honey bee lineage. Our results confirm that population-specific genetic markers should always be evaluated in a new population prior to using them in MAS programs.
... The brood investigation required for this is tedious 15 and the accuracy of MNR and REC values strongly depends on sample size 22 . Since MNR seems to be the outcome of different background mechanisms 10 , it shows a low phenotypic repeatability compared to REC and other resistance traits [22][23][24] . However, these changes might simply be linked to seasonal differences in the expression of underlying behaviours (e.g., VSH or REC) due to changing nectar flows 25 , brood rearing activity 26 or other unknown factors. ...
... 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.
... The varroa mite remains one of the greatest threats to honey bee health and causes widespread colony losses of A. mellifera 13 , especially in winter. Breeding and selection programs worldwide seek a sustainable approach to control the mite and are thus attempting to breed varroa tolerant or resistant stock using a variety of different selection criteria [14][15][16] . Hygienic behaviour towards mite infested brood cells has been identified as a biological method to reduce mite infestation levels in colonies 17 . ...
Varroa destructor is one of the main causes of colony losses of the western honey bee (Apis mellifera). Many efforts exist to breed honey bees resistant to V. destructor. Varroa sensitive hygiene (VSH) is a commonly selected behavioural trait; VSH workers remove the pupae of mite infested brood cells with high efficiency, interrupting the reproduction of the mite. The cues and triggers for this behaviour are not yet fully understood. To determine what elicits this removal behaviour, we examined preselected VSH workers´ responses to four different groups of objects inserted into freshly capped cells: live mites, dead mites, odour reduced mites, and glass beads. These were also compared to control cells that were opened and closed without inserting any object. The pupae in cells containing inorganic objects (glass beads) were removed at similar rates to the control, demonstrating that an object alone does not trigger a removal response. Dead and odour reduced mites were removed at a higher frequency than control cells, but less frequently than live mites. Workers sometimes removed items resting near the top of the cell without removing the pupa. Our results demonstrate that although mite odour from dead mites triggers removal behaviour, the pupa of cells containing live mites were removed more frequently, suggesting that other cues (i.e. odour from feeding wound) or signals (i.e. pupal movement to signal distress) are important. Future research should focus on elucidating these other cues or signals from the brood and mites, as mite presence alone seems to be insufficient.
... For example, a lower reproductive success of mites was frequently reported for naturally surviving colonies (Grindrod and Martin 2021;Locke 2016;Oddie et al. 2018). Thus, this phenomenon is regarded as a selection criterion for breeding towards Varroa resistance (Büchler et al. 2010(Büchler et al. , 2020aMondet et al. 2020b), often measured after artificial infestation with mites gained from broodless donor colonies. Hence, such measurements on colony level might be distorted, if the expression of reproductive failure per se would be altered by brood interruptions. ...
The parasitic mite Varroa destructor (Anderson & Trueman) spends the dispersal phase of its life cycle on adult honeybees ( Apis mellifera L.). The meaning of this phase for both bees and mites is still not well understood. This especially applies to prolonged dispersal phases as a result of brood interruptions. Hence, it is highly important to unravel this phase for understanding the underlying biological mechanisms and implementing this knowledge in beekeeping practice and research efforts. We investigated the effects of brood interruptions on honeybee colonies and the mites naturally infesting them. Reproduction parameters, brood infestation and recapping frequency were monitored over 60 days after brood interruptions of varying durations. Our results show that recapping frequency and mite non-reproduction increased during the interruption of egg laying. The duration of interruption and the time elapsed afterwards additionally affected the occurrence of reproductive failure. Hence, the reproduction of mites was affected by brood breaks immediately and in the long run.
... Apart from technology transfer, agricultural research and extension should meet new demands, food security, and rural poverty alleviation (Waithaka 2001). Global experience on apicultural research shows that the focus has been evolving from improving productivity and temperament (Adam 1987) to vitality and local adaptation (Blacquière et al. 2019;Büchler et al. 2020); gearing to address massive challenges of V. destructor (Conte et al. 2020) and genetic erosion (Espregueira Themudo et al. 2020). Traditionally, beekeepers in Tigray select colonies based on colony size (strength), color, gentleness, honey yield, etc. ...
Subsistent beekeeping has been an established tradition in Tigray, northern Ethiopia. In the last two decades, extension efforts tried to transform it into improved apiculture, which led to development of colony marketing. Here, we assessed the progress in beekeeping, colony marketing, and population differentiation with a hypothesis that the extension might have supported both production and genetic conservation in accordance with the national apiculture proclamation. Progress in beekeeping was analyzed based on official annual reports from 2004 to 2020. In addition, colony market survey was conducted in one of the central markets to analyze spatial and agro-ecological zone (AEZ) distributions of the honey bees, driving factors, and implications by interviewing 120 sellers and buyers. Moreover, highland and lowland honey bee population differentiation was compared in two areas (not-) involved in marketing using a nuclear marker known for elevational adaptation. The regional beekeeping progressed substantially: frame hives grew from 1 to 23%, annual honey production tripled, managed colonies increased by 90%. Frame hives provided significantly (F = 88.8, P < 0.001) higher honey yield than local hives. Colonies were exchanged between actors with significant differences in spatial (X 2 = 104.56, P < 0.01) and AEZ (X 2 = 6.27, P = 0.044) distributions. Colonies originate mainly from highland areas of two districts and were redistributed to broader areas. Most buyers showed preferences for colony color (73.3%) and AEZ of origin (88.3%), which led to a one-way flow. Consequently, no genetic differentiation was detected between two contrasting elevations in the involving district compared to a not involving area (F ST = 0.22). Overall, the regional apiculture progressed significantly, but there is no evidence that the extension contributed to conservation. apiculture / population genetics / sustainable development / tigray
... A common trait used for selection is suppressed mite reproduction (SMR; Büchler et al. 2010, Rinderer et al. 2010, Guichard et al. 2020a. SMR is phenotyped using two methods: the assessment of mite fecundity by counting the number of viable daughters produced (e.g., Martin 1994Martin , 1995Martin , 1997, or of mite infertility, as the lack of mite reproductive success expressed as the percentage of mites producing no viable daughters (Büchler et al. 2020, Eynard et al. 2020, Mondet et al. 2020b. The reduction in mite reproduction by SMR is thought to result from the properties of immature (i.e., brood) or adult hosts (Harbo and Harris 2005, Conlon et al. 2019. ...
... DMR has frequently been implemented in selection programmes, showing its popularity amongst honey bee breeders (Guichard et al. 2020a) and leading to an increase in published reports. These reports allowed for first estimates of the effectiveness of selecting this trait toward resistant honey bee lineages (DeGrandi-Hoffman et al. 2002, Büchler et al. 2020, Eynard et al. 2020, Guichard et al. 2020a. Several limitations in using DMR appeared, hindering its practical implementation (Guichard et al. 2020a). ...
... Recording DMR phenotypes late during the colony evaluation process leads to a generation time of two years in colonies selected for this trait in temperate regions, only allowing for slow genetic progress. The literature on DMR also indicates that infertility-based measures have low repeatability and are imprecise (Büchler et al. 2020, Eynard et al. 2020. The poor repeatability has been attributed to varying environmental conditions between measurement times (Büchler et al. 2020, Eynard et al. 2020). ...
The invasive parasitic mite, Varroa destructor (Anderson and Trueman), is the major biotic threat to the survival of European honey bees, Apis mellifera L. To improve colony survival against V. destructor, the selection of resistant lineages against this parasite is considered a sustainable solution. Among selected traits, mite fertility and fecundity, often referred to as suppressed mite reproduction are increasingly used in breeding programmes. However, the current literature leaves some gaps in the assessment of the effectiveness of selecting these traits toward achieving resistance. In the population studied here, we show a low repeatability and re-producibility of mite fertility and fecundity phenotypes, as well as a low correlation of these traits with infestation rates of colonies. Phenotyping reliability could neither be improved by increasing the number of worker brood cells screened, nor by screening drone brood, which is highly attractive for the parasite and available early in the season, theoretically allowing a reduction of generation time and thus an acceleration of genetic progress in selected lineages. Our results provide an evaluation of the potential and limitations of selecting on decreased mite reproduction traits to obtain V. destructor-resistant honeybee colonies. To allow for a more precise implementation of such selection and output reporting, we propose a refined nomenclature by introducing the terms of decreased mite reproduction and reduced mite reproduction, depending on the extent of mite reproduction targeted. We also highlight the importance of ensuring accurate phenotyping ahead of initiating long-lasting selection programmes.
... For example, an imbalance of 'uncapper' versus 'recapper' bees may cause many brood cells to be left open [55]. Consequently, it can be very hard to accurately measure resistanceassociated traits [117,118,129], resulting in a high degree of variability within colonies and across colony-level datasets ( figure 1b,c,e). Ultimately, variability severely affects selection programmes (reviewed in [130]), whereas in natural selection-based experiments such as bond experiments [15] and black box experiments [13,131], assumptions on the importance of traits are not made. ...
The near-globally distributed ecto-parasitic mite of the Apis mellifera honey-bee, Varroa destructor, has formed a lethal association with Deformed wing virus, a once rare and benign RNA virus. In concert, the two have killed millions of wild and managed colonies, particularly across the Northern Hemisphere, forcing the need for regular acaricide application to ensure colony survival. However, despite the short association (in evolutionary terms), a small but increasing number of A. mellifera populations across the globe have been surviving many years without any mite control methods. This long-term survival, or Varroa resistance, is consistently associated with the same suite of traits (recapping, brood removal and reduced mite reproduction) irrespective of location. Here we conduct an analysis of data extracted from 60 papers to illustrate how these traits connect together to explain decades of mite resistance data. We have potentially a unified understanding of natural Varroa resistance that will help the global industry achieve widespread miticide-free beekeeping and indicate how different honeybee populations across four continents have resolved a recent threat using the same suite of behaviours.
