Bumblebee worker reproduction as an independent test of Haig's kinship theory for the evolution of genomic imprinting

Lead Research Organisation: University of Leicester
Department Name: Biology

Abstract

This project will independently test the major theory for the evolution of genomic imprinting, by examining the parent of origin allele specific expression of genes important for bumblebee worker reproduction. My group has pioneered the study of both worker reproduction gene expression and allele specific expression in bumblebees.

Genomic imprinting is the differential expression of alleles in diploid individuals, with the expression being dependent upon the sex of the parent from which it was inherited. It is an important area of research in evolutionary biology, in human health (cancers and developmental syndromes) and in plant breeding. Haig's kinship theory is the leading theory explaining the evolution of genomic imprinting. It predicts that genes that are upregulated when queenless bumblebee workers reproduce should be more expressed from the allele from the mother (matrigene). The reciprocal is also predicted, that genes upregulated in non-reproductive workers should be patrigenically (allele from the father) expressed. As, so far no imprinted genes have been discovered in bumblebees, this project is a truly independent test of a major evolutionary theory.

In order to test Haig's kinship theory we need to deliver three aims:-
* produce queenless reproducing workers from maximally heterozygous reciprocally crossed bumblebee colonies.
* identify candidate imprinted genes in queenless reproductive workers.
* test the predictions of Haig's kinship theory that imprinted genes that are upregulated in queenless reproductive workers should be matrigenically expressed and that imprinted genes that are upregulated in non-reproductive workers should be patrigenically expressed.


The proposed project will use whole transcriptome sequencing (RNA-seq) to examine the matrigenic and patrigenic expression of known worker reproduction genes in the bumblebee, Bombus terrestris in order to test Haig's theory for the evolution of genomic imprinting.

We will achieve our aims by carrying out three objectives:-
* We will use established breeding techniques and genetically distant colonies in order to produce ten heterozygous reciprocally crossed bumblebee colonies from each of which we will collect six queenless reproducing workers.
* We will analyse RNA-seq libraries of the brains of three reproducing workers from each of these ten colonies in order to identify candidate imprinted genes in queenless reproductive workers.
* We will measure, using an independent technique, the allele specific expression of candidate imprinted genes in three further reproducing workers per colony, in order to test the predictions of Haig's kinship theory.


This project is "an unusual opportunity for a truly blind test of a sociobiological theory" (Queller 2002). We will publish our results in peer reviewed journals and present them at international conferences. All datasets will be made available on public databases.

Planned Impact

We expect that the specific users and beneficiaries of our research (outside of the academic community) will be environmental operators, leaders of commerce, policymakers, educators and, more widely, the general public. We will engage with these groups using different methods of disseminating information which will be facilitated by GENIE (Genetics Education Networking for Innovation and Excellence). GENIE is a Centre of Excellence in Teaching and Learning (CETL) which is run by Prof Annette Cashmore in the Department of Genetics

Bumblebee breeding is an important industry in Europe. Our results may allow more efficient production of males and females. The University of Leicester has a vigorous and experienced "Enterprise & Business Development" team and an embedded unit ("The Biobator"), dedicated to exploitation of activities arising from work in biological research. In year 1 we will arrange a calendar of engagement sessions with The Biobator to discuss potential commercial applications of the research and to train project staff in knowledge transfer (KT) skills. Biobator staff will arrange appointments, aid us in seeking industrial partners, publicize and negotiate with regional organisations and seek opportunities for consultancy and KT activities.

Publications

10 25 50

 
Description For most genes in our body we have two copies. One we got from our mother, the other from our father. Normally these are both used or "expressed". However, for a few genes in our body, only the mother's or the father's version is used. This phenomenon is called genomic imprinting. It is common throughout mammals and flowering plants. It is an important process in some developmental syndromes (e.g. Prader-Willi) and cancers.

Our group recently found some genes in the bumblebee that behave like this. We found that some genes use the mother's version and some genes use the father's version more. This is very exciting and further study will tell us many things about how genomic imprinting evolved, its commonalities between these distantly related groups, and its effect on this important pollinator's biology.

This last part is particularly important. Bumblebees are among the most important wild pollinators in the temperate Northern Hemisphere and at least 25 major crops grown within the EU are visited by bumblebees. Collectively, insect pollination services are worth 14.2 billion euros to Europe's economy. In the UK, 52% of the surveyed areas have experienced a decline in bee-species richness since 1980. Eleven percent of bumblebee species are listed as 'near threatened' or above using the IUCN Red List criteria.
Exploitation Route How imprinting happens in us is reasonably well understood. However, for our bees, there is no clear mechanism to explain how imprinting could work. This project will begin to elucidate a mechanism for genomic imprinting in these bees. There are two mechanisms that the human body uses to imprint genes that bees also possess; DNA methylation and histone methylation. A methyl group is a carbon and three hydrogen atoms. When you attach this to DNA, it affects how the DNA is expressed. Histones are how DNA is packaged in our cells. Attaching a methyl group to a part of a histone changes its shape, which can change whether the gene it contains is expressed or not.
Sectors Agriculture, Food and Drink,Environment

 
Description How do bees imprint genes?
Amount £194,432 (GBP)
Funding ID RPG-2020-363 
Organisation The Leverhulme Trust 
Sector Charity/Non Profit
Country United Kingdom
Start 06/2021 
End 05/2024
 
Title The effect of DNA methylation on bumblebee colony development 
Description Abstract Background Although around 1% of cytosines in bees' genomes are known to be methylated, less is known about methylation's effect on bee behavior and fitness. Chemically altered DNA methylation levels have shown clear changes in the dominance and reproductive behavior of workers in queen-less colonies, but the global effect of DNA methylation on caste determination and colony development remains unclear, mainly because of difficulties in controlling for genetic differences among experimental subjects in the parental line. Here, we investigated the effect of the methylation altering agent decitabine on the developmental rate of full bumblebee colonies. Whole genome bisulfite sequencing was used to assess differences in methylation status. Results Our results showed fewer methylated loci in the control group. A total of 22 CpG loci were identified as significantly differentially methylated between treated and control workers with a change in methylation levels of 10% or more. Loci that were methylated differentially between groups participated in pathways including neuron function, oocyte regulation and metabolic processes. Treated colonies tended to develop faster, and therefore more workers were found at a given developmental stage. However, male production followed the opposite trend and it tended to be higher in control colonies. Conclusion Overall, our results indicate that altered methylation patterns resulted in an improved cooperation between workers, while there were no signs of abnormal worker dominance or caste determination. 
Type Of Material Database/Collection of data 
Year Produced 2021 
Provided To Others? Yes  
Impact Allowed for publication of paper 
URL https://springernature.figshare.com/collections/The_effect_of_DNA_methylation_on_bumblebee_colony_de...
 
Title supplementary data for manuscript "The neonicotinoid, imidicloprid affects gene expression and methylation in the buff-tailed bumblebee Bombus terrestris" 
Description Various datasets related to manuscript "The neonicotinoid, imidicloprid affects gene expression and methylation in thebuff-tailed bumblebee Bombus terrestris" 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
Impact Allowed for publication of paper 
URL https://figshare.com/articles/supplementary_data/6796802/5
 
Description The battle of the sexes in bumblebees 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? Yes
Geographic Reach Regional
Primary Audience Public/other audiences
Results and Impact A talk to various local groups based on the findings from this grant.
Year(s) Of Engagement Activity 2017,2018,2019