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Social immunity and Hygienic Behaviour

Dave Black

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Social insects like honeybee living in close proximity have a higher risk of spreading diseases and poisons among nestmates, so we would expect to find mechanisms that mitigate this. One of these systems is an innate immune system that provides an antimicrobial film on their exoskeleton, a hostile gut environment, a peritrophic membrane and gut epithelium, and effective cellular and humoral defences. These secrete antimicrobial chemicals, engulf or entomb foreign materials, and provide enzymes that degrade or destroy pesticides and pathogens. The genetic precursors for all this are ancient, common to invertebrates and invertebrates, and consequently fairly well understood.

If we compare honey bees to other solitary insects we find that, relatively, honey bees have about a third as many of the genes known to be associated with disease immunity. Partly that is likely to be because they are targeted by fewer, more specialist pathogens, and live in a very stable nest environment, but it’s also because they use a highly developed strategy that combines behavioural traits that together provide a social immunity. Collectively, they construct or maintain nests using antimicrobial materials, keep their young in hygienic, homeostatic, sterile nurseries, create a ‘fever’ in response to disease, functionally exclude foraging bees from parts of the nest, groom, exhibit ‘altruistic’ suicide, and delegate risk-taking to expendable members of the group. These behavioural traits seem particularly important and yet we know very little about them, how they work, and how they are inherited, even after decades of ‘trial & error’ field research has shown that they are highly effective and highly inheritable.

A group of researchers in Canada are involved in a long-running project studying the basis for inheritance of this social immunity. The scale and duration of the study differentiates it from most. Their most recent paper was just published last month.

For this study they created two selected populations (of 100 colonies each) that express hygienic behaviour (using freeze-killed brood) across three generations relative to a ‘baseline’ 100 colony population (control). They used genome sequencing to identify genetic ‘loci’ that were associated with the variation in behaviour. The genome sequencing allowed them to consider 2,340,950 SNPs. (Think of SNPs as alterations in DNA sequences – a person will have four to five million SNPs in their genome).

The researchers identified regions in the genome that differed between the study and control group down the generations, homing in on 10,140 SNPs, and then compared their candidates to six other, independent studies which at first zeroed in on 2,058 SNPs in 99 regions in the genome, and they then refined that to 73 protein-coding genes that looked to be the most significant in terms of hygienic behaviour. Usefully, perhaps surprisingly, 85-90% of these genes were not unique to honey bees but are shared with other hymenoptera and insects in general. These genes are already all known to be associated with the functioning of features of the neurological system, for example in nerve growth and signal transmission, and olfaction. Rather than novel genes being responsible for hygienic behaviour, it seems that existing genes and gene networks are conserved and ‘repurposed’ during adult development or maturation, perhaps by a difference in the regulation of a pre-existing ‘tool-kit’. But keep that 73 genes in mind. The authors also claim that the ancient genetic ancestry of their selected, hygienic genes had much more in common with C-lineage (Central European) Apis bees (ligustica; carnica) than M-lineages (mellifera) or O, A, Y (Mid-East, Africa, or Yemen, Saudi). This is interesting because many other studies (six are mentioned) have independently come to the same conclusion, that C-lineage bees (carrying C-lineage genes) have superior hygienic abilities.

This is the fourth paper in this vein from this group so far. They began (2010) by looking for signs of local adaption in honey bees, establishing and comparing populations from within Canada, but also including some from Chile, California, Hawaii, and Hawkes Bay, because that was where they were buying queens and packages from. They were interested in seeing what trade-offs were being made, if any, by the necessary import of, possibly, mal-adapted stocks. They were able to show distinct metabolic adaptions that related to the geographical source; in some respects, metabolically, NZ bees had more in common with Chilean bees that with Canadian bees. In their words, “The populations studied… may represent separate geographical ecotypes, where metabolic control and protein synthesis/folding mechanisms has been finely tuned to confer fitness to local environmental pressures such as climate, food resources, predation and diseases.”

The second paper released (2015) used a subset of the same bee population (without the NZ bees as far as I can tell) to see if it would be possible to use molecular markers rather than behavioural tests to select more disease resistant stock, since that would be faster. They suggest biomarkers in the form of the expression of a particular set of proteins would be a better tool than conventional Marker-Assisted-Selection (They looked specifically at odorant-binding proteins in antennae that correlated with hygienic behaviour). The third paper (2017) has a more detailed demonstration of an ‘expression marker’ as they call it, successfully testing the idea against AFB and varroa in a selection and breeding programme lasting three years. This is how they sum up that paper;

“[Marker Assisted Selection - MAS] has the potential to be more precise and more robust to external influences; it has been widely used in certain plants and animals. To date, however, the markers used have been genomic loci exclusively...undoubtedly due, in part, to the availability of efficient genetic approaches for finding such markers. It is also a matter of focus: researchers have spent more time looking for genetic loci than for expression markers... Here we have shown that expression markers can be used to select for a very complex, polygenic trait. (Remember the 73 genes?) Even in this proof-of-principle with a first-generation panel of markers, MAS was as efficient at enriching disease-resistance as Field Assisted Selection [FAS] methods: bees bred using marker-assisted selection could resist levels of disease that would typically kill 70% or more of unselected colonies. The data presented here have implications beyond bees: this is the first demonstration of marker-assisted selection in livestock using expression markers and it enables molecular diagnostic approaches for selecting complex polygenic traits that are recalcitrant to genetic mapping methods. After three generations of selection, the resulting marker-selected stock outperformed an unselected benchmark stock in terms of hygienic behaviour (sic), and had improved survival when challenged with a bacterial disease or a parasitic mite, similar to bees selected using a phenotype–based assessment for this trait. This is the first demonstration of the efficacy of protein markers for industrial selective breeding in any agricultural species, plant or animal.”

Just because I can - it seems to be a major topic of discussion at the moment, I’m going to note how all this was funded; a muti-site, international, nine year project using several hundred colonies and some expensive, novel, lab work. Here is a list of the bill-payers;

Genome British Columbia, the British Columbia Honey Producers Association,  the Canadian Honey Council and Canadian Association of Professional Apiculturists through the Canadian Bee Research Fund, the British Columbia Blueberry Council, the British Columbia Cranberry Marketing Association, Agri-Food Canada’s Advancing Canadian Agriculture and Agri-Food (ACAAF) program, Ontario Genomics, a Discovery Grant from the Natural Sciences and Engineering Council (NSERC) of Canada,  Genome British Columbia, Genome Alberta, the University of British Columbia, the University of Manitoba, and the US Department of Agriculture. I haven’t included odd scholarships or research grants supporting the tenure of individuals.

Food for thought.

 

Brock A. Harpur, M. Marta Guarna, Elizabeth Huxter, Heather Higo, Kyung-Mee Moon, Shelley E. Hoover, Abdullah Ibrahim Andony P. Melathopoulos, Suresh Desai, Robert W. Currie, Stephen F. Pernal, Leonard J. Foster, and Amro Zayed. (2019) Integrative genomics reveals the genetics and evolution of the honey bee’s social immune system. Genome Biol Evol. 2019 Feb 15.  doi: 10.1093/gbe/evz018

Guarna MM, et al. 2017. Peptide biomarkers used for the selective breeding of a complex polygenic trait in honey bees. Scientific Reports 7: 8381.

Guarna MM, et al. 2015. A search for protein biomarkers links olfactory signal transduction to social immunity. Bmc Genomics 16: 63. doi: 10.1186/s12864-014-1193-6

Parker R, Melathopoulos AP, White R, Pernal SF, Guarna MM, Foster LJ. (2010) Ecological adaptation of diverse honey bee (Apis mellifera) populations. PLoS One. 2010;5(6):e11096.

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Can you please summarise the summary ? 

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Awsome Dave, so good to here from you again always love your posts I haven't been here much lately, but always appreciated your input and your knowledge, we must catch up sometime 

Also I would expect nothing less than a post like this from you haha, your a legend.

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