Category: Articles

New Paper: Population Genomics of the Honey Bee in PNAS

By , February 26, 2014

Hi All,

harpur2014_coverI am very happy to announce the publication of a new paper from the lab, which appeared last week in the Proceedings of the National Academy of Sciences (PNAS) – a top journal in the field.  The study was featured on the cover of PNAS, and received a highlight in the “In This Issue” section of the journal.  Also see York U’s press release on the article.

The article was co-first authored by PhD Candidate Brock Harpur and postdoctoral fellow Dr. Clement Kent, with further contributions from MSc candidate Daria Molodostova, former Research at York undergraduate Jonathan Lebon, and two collaborators from King Saud University, Drs. Abdualziz Alqarni and Ayman Owayss.

The study involved sequencing the genomes of 39 European honey bees (Apis mellifera) from their native range in Africa, Asia, and Europe. We also sequenced the genome of the Asiatic honey bee Apis cerana.  We were able to identify over 12 million mutations in the European honey bee and this allowed us to identify DNA regions that have experienced positive ‘Darwinian’ selection. Positive selection refers to the evolutionary process that increase the frequency of beneficial mutations in a population, because such mutations confer an advantage to the individuals carrying them (e.g. such individuals can survive better, or reproduce more relative to others in the population).

Studying selection in social insects is not straight forward because worker honey bees are effectively sterile – they do not have offspring of their own, so they can only experience positive selection indirectly; mutations that affect a worker’s helping behaviour can only spread through the population if the helping behaviour allows their mother queen to produce more queens and drones (reproductive male bees); this is called kin-selection.  We set out to look for evidence of kin selection by searching for signs of positive selection on genes and proteins that affect worker traits.  We find very strong evidence that genes associated with worker behaviour experience high rates of positive selection. These included Royal Jelly proteins, which are produced in specialized worker glands to feed their sisters. Indeed, the gene for royalactin, the royal jelly that workers feed to young larva to make them queens, shows very high rates of positive selection.

We also found that worker biased proteins (i.e. proteins that are expressed at higher levels in workers relative to queens) experience stronger positive selection than queen-biased proteins.

The y-axis here is Y, a measure of the strength of selection (positive values indicate positive selection). We found that worker biased proteins have higher levels of selection relative to queen biased proteins, as well as proteins that are not differentially expressed between queens and workers (NDEG). Figure reproduced from our PNAS paper

The y-axis here is Y, a measure of the strength of selection (positive values indicate positive selection). We found that worker biased proteins have higher levels of selection relative to queen biased proteins, as well as proteins that are not differentially expressed between queens and workers (NDEG). Figure reproduced from our PNAS paper

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Our study shows that workers, through their helping behaviour, play a major role in environmental adaptation in the honey bee.  In other words, ‘survival of the fittest’ in honey bees is essentially survival of the colonies with the best workers!

Cheers,
Amro

PNAS Cake II

By , January 7, 2014

Very happy to report that, after months of hard work, we’ve just heard that our study will be published in PNAS – a top science journal. Can’t tell you much about the article now – it is embargoed until published – but it is very very neat in my humble and biased opinion. We had a little mini-celebration with PNAS cake… Yum! 🙂

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Hmmm, 40^3!

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[L to R]: Nadia, Alivia, Jen, Daria, Phil, Brock, Lior, Amro

Management and diversity in honey bees: comment and reply.

By , June 2, 2013

De la Rúa et al. raised some comments about our recent article showing that management enhances genetic diversity in honey bees. Their comments, along with our response have been published online in Molecular Ecology.  We stress that admixture does enhance genetic diversity in managed bees.

Conserving genetic diversity in the honeybee: Comments on Harpur et al. (2012)
Pilar De la Rúa, Rodolfo Jaffé, Irene Muñoz, José Serrano, Robin F. A. Moritz and F. Bernhard Kraus
Article first published online: 28 MAY 2013 | DOI: 10.1111/mec.12333

and

Admixture increases diversity in managed honey bees: Reply to De la Rúa et al. (2013)
Brock A. Harpur, Shermineh Minaei, Clement F. Kent and Amro Zayed
Article first published online: 9 MAY 2013 | DOI: 10.1111/mec.12332

New paper: the curious case of the disappearing immune genes in honey bees.

By , April 9, 2013

We have a new paper out in Molecular Biology and Evolution.  See the press release here.

When the honey bee Apis mellifera genome was sequenced in 2006, researchers found that the bee has fewer innate immune genes – the genes that recognize and destroy pathogens – than other solitary insects.  The bee had about 30% of the innate immune genes found in flies and mosquitos.  Wow! Why?

Dr. Jay Evans (USDA) and colleagues hypothesized that maybe bees have fewer pathogens, or that they can fight pathogens better with social behaviour; worker bees can groom themselves and their sisters, and they can recognize sick/dead larva and remove them from the colony.

Brock Harpur, a MSc (now PhD) student in the lab is very interested in immunity in social insects, and he decided to study the evolution of 13 innate immune genes in the honey bee.  We sequenced these genes in about 40 different honey bee workers, and in one worker of the closely related Asian honey bee Apis cerana.  This allowed us to discover mutations in innate immune genes within the European honey bee Apis mellifera, and between the European and the Asian honey bee (Apis mellifera vs. Apis cerana).  We compared the amount of mutations in innate immune genes to those found in 20 randomly chosen genes.

The DNA sequence of a given gene codes for a specific sequence of amino acids that get folded into a 3-dimensional protein that then preforms a specific function within the cell.  Mutations in a gene sequence come in two flavours: there are mutations that don’t change the amino acid sequence of the resulting protein (we call these silent mutations), and there are mutations that change the amino acid sequence of the resulting protein (we call these replacement mutations).  The silent mutations – because they do not affect the shape and structure of the resulting protein – do not often affect fitness and are not ‘weeded-out’ by natural selection; silent mutations accumulated within species, and between species.  However, replacement mutations will change the shape / structure of proteins, and often the resulting protein will not function optimally (if it works at all).  These mutations, because they are often bad, are then rapidly removed by natural selection (because bees with these mutations do not survival as well).

Now imagine a gene sequence that was functional in an ancestor but is now no longer necessary.  Replacement mutations in such genes will no longer be weeded-out by natural selection (because bees with these mutations survival normally), and these mutations can then accumulate similar to silent mutations; this process is called ‘relaxation of purifying selection or relaxation of constraint’.

 

When selection is relaxed (right), mutations accumulate at fast rates in gene sequences. Normally, mutations that alter the amino acid sequence of a protein will be removed by purifying selection as a large fraction of these mutations are bad (left)

 

 

 

 

 

 

 

 

 

 

 

This is exactly what we see when we look at most immune genes in the honey bee. When we examine silent mutations, immune genes and random genes have similar rates. However, if we examine replacement mutations, we find that immune genes have 3 to 4 higher mutations relative to random genes; this is consistent with a relaxation of purifying selection.  We reckon that the same process that resulted in massive loss of innate immune genes in the bee is still acting to erode some of the remaining innate immune genes in contemporary bee populations.  Our work supports Dr. Jay Evans’ idea that some aspect of social living makes an individual-based innate immune system less useful.

New paper: the evolution of recombination rates in social insects

By , March 25, 2013

We have a paper out this month in Communicative and Integrative Biology on the evolution of recombination rates in social insects.  This follows up on our recent PNAS paper showing a relationship between recombination, GC content, and worker biased genes in the honey bee.  We now present a conceptual paper on how high recombination could have been advantageous during the initial stages of the evolution of sociality, which in turn could have affected GC content in social insects.  The paper was authored by Dr Clement Kent – a postdoctoral fellow in the lab.  Its an open access article, so you can download it and read it for free!

Amro

Recombination, GC, and worker behaviour: comment and reply.

By , February 5, 2013

Our colleagues Drs. Hunt, Glastad, and Goodisman raised some comments about our recent article showing a relationship between recombination, GC content, and worker-baised genes in honey bees;  Their comments, along with our response were published online this week in the Proceedings of the National Academy of Sciences.

Genome composition, caste, and molecular evolution in eusocial insects
Brendan G. Hunt, Karl M. Glastad, and Michael A. D. Goodisman
PNAS 2013 110 (6) E445-E446; published ahead of print February 1, 2013, doi:10.1073/pnas.1220586110

and

Reply to Hunt et al.: Worker-biased genes have high guanine–cytosine content and rates of nucleotide diversity in the honey bee
Clement F. Kent, Shermineh Minaei, Brock A. Harpur, and Amro Zayed
PNAS 2013 110 (6) E447; published ahead of print February 1, 2013, doi:10.1073/pnas.1221223110

 

New Faculty of 1000 recommendation

By , November 27, 2012

Dr. Nicolas Galtier from the Institut des Sciences de l’Evolution, Université Montpellier II, Montpellier, France, recommended our recent PNAS article on recombination and evolution in honey bees on Faculty of 1000 . Check it out! Access the recommendation on F1000 Prime

New Paper: A review on Brain Gene Expression and Behaviour

By , November 20, 2012

I am very happy to announce the recent publication of a collaborative review on the relationship between brain gene expression and behaviour with Dr. Gene Robinson at the University of Illinois.  We reviewed a large number of studies examining changes in brain gene expression in the honey bee across a wide spectrum of behaviours,  environments, and honey bee subspecies.

We showed that brain gene expression is intimately linked to behaviour and that changes in brain gene expression bring about changes in behaviour.  We discuss how changes in the environment as well as changes in physiology affect bee behaviour by first affecting brain gene expression.  Finally, we showed that the association between specific genes and behaviour can be highly conserved over evolutionary time, leading to common basis of behaviour across distantly related animals.

The review appeared last week in Annual Review of Genetics

Zayed A, Robinson GE (2012) Understanding the relationship between brain gene expression and social behavior: Lessons from the honey bee. Annual Review of Genetics 46, 591-615.

New Paper: Recombination and Honey bee evolution

By , October 30, 2012
We are very happy to announce a new and very exciting paper from the lab – recently published by the Proceedings of the National Academy of Science. [see also Press Release and PNAS Cake!]
The honey bee genome has two unusual properties. First – it has the highest recombination rate in animals: Recombination shuffles the genetic deck by mixing up the chromosomes inherited from parents into offspring. Recombination makes the actions of natural selection more efficient because it allows beneficial mutations to spread irregardless of the effects of nearby mutations (see Fig 1).

Fig. 1. Recombination shuffles ‘parental chromosomes’ (red and blue), generating ‘mosaic’ or recombined chromosomes. This is how recombination makes natural selection act more effectively: Lets imagine a new beneficial mutation occurring nearby a deleterious (=bad) mutation on the blue chromosome. With no (or low) recombination, the two mutations would be stuck together… forever… and this would prevent natural selection from removing the bad mutation and spreading the good mutation. But if recombination generates a new mosaic chromosome that has the good mutation but not the bad mutation (as pictured), then the good mutation can spread by natural selection!

 Second – the bee’s genome has areas that are very rich in the DNA bases G and C, while other areas are very rich in the bases A and T.
Our paper showed that these high GC and low AT genomic regions are maintained by differences in the recombination rate across the bee’s genome: areas with low recombination move towards high AT and areas with high recombination move toward high GC – because of a phenomenon called GC-biased gene conversion.  This biased gene conversion is a side effect of high recombination and it acts by increasing the frequency of G or C mutations over A or T mutations.
We also found that regions of the bee genome with high rates of recombination and high GC content have more genetic diversity and evolve a lot faster than genomic regions with low recombination and high AT content.
Now, here comes the fun part… what kind of genes ‘live’ in these high GC genomic areas that have high rates of evolution ?  We first looked at high GC genes and examined their biological function in other organisms – turns out many were involved in brain function and things like learning and memory.  This is interesting because we know that worker bees (and workers in other social insects) have some of the coolest behaviours out there (remember… they dance!).  So we went back to the literature and found several lists of genes that get turned ‘on’ in the brains of workers relative to the brains of queens and drones [Check out Drones are from Mars, Workers are from Venus!].  It turns out that worker-associated genes are predominantly GC rich, while queen- and drone- associated genes are predominantly AT rich.

Worker ‘genes’ are GC rich baby! Fig 2 from our PNAS paper, in both tiff and cake formats. The Tiff format is more impactful but the cake format is tastier

So, our results show that the bee’s high recombination rate increases the evolutionary rate of genes associated with worker behaviour, which is an important finding because worker behaviour plays a major role in determining the fitness of insect colonies.

The paper was authored by postdoctoral fellow Dr. Clement Kent, and former Masters students Shermineh Minaei and Brock Harpur.

 

[edit March 2013].  See Faculty of 1000 recombination, comment by Hunt et al and our reply, and addendum in Communicative and Integrative Biology

PNAS Cake

By , September 19, 2012

Today was a fine day.  We had a very important paper from the lab accepted in Proceedings of the National Academy of Sciences (PNAS), one of the top journals in our field.  I can’t tell you much about the work for now – it is embargoed until officially published by the journal – other than… it is very very very cool!  But, perhaps you can guess the topic after seeing our ‘PNAS Cake”! [feel free to send your guesses via the comment box below]

The cake-lady at highland farms had a good chuckle when i handed her fig. 2 of our manuscript at 8:45 am today 🙂

 

 

 

 

 

 

 

 

 

 

 

The paper, and tasty cake, were the results of massive efforts by postdoctoral fellow Dr. Clement Kent, with the help of  Shermineh Minaei and Brock Harpur (the latter two are recently minted MSc’s).

L-R: Brock, Amro, Clement, Nadia, Tabashir, Arash, Anna