Worker rebellion: a role for imprinted genes in bumblebees?

We don’t just inher­it DNA from our par­ents, we also inher­it chem­ic­al marks which can tell our genes how to behave. These marks can some­times make our genes work in a way that goes against tra­di­tion­al evol­u­tion­ary under­stand­ing. A new study in Evol­u­tion Let­ters explains how bumble­bees may hold the key to val­id­at­ing new the­or­ies around the evol­u­tion of these weirdly behav­ing genes.

Most anim­als, includ­ing you, inher­it two cop­ies of their DNA, one from mum and one from dad. This means we have two cop­ies of every gene, a mater­nal copy (from mum) and a paternal copy (from dad). Usu­ally both cop­ies of a gene are expressed, mean­ing they are turned on. This is evol­u­tion­ar­ily import­ant because if you were to inher­it a dam­aged copy of a gene, then the oth­er healthy copy can some­times com­pensate. How­ever, there are a small num­ber of genes that lose this evol­u­tion­ary advant­age by only ever express­ing one copy. When this is done in a par­ent-of-ori­gin man­ner, the genes are referred to as imprin­ted. This means some imprin­ted genes only ever express dad’s copy and oth­ers only ever express mum’s copy. For example, in humans, it is only ever the paternal copy of the IGF2 gene that gets expressed. If imprint­ing is lost at this gene it res­ults in Beck­with-Wie­der­mann syn­drome, which can cause giant­ism and excess tumour growth.

Why has gen­om­ic imprint­ing evolved?

Gen­om­ic imprint­ing is an evol­u­tion­ary para­dox as nat­ur­al selec­tion should not favour the switch­ing off of one copy of a gene. Many the­or­ies try to explain why gen­om­ic imprint­ing has evolved. Haig’s kin­ship the­ory is the most widely accep­ted explan­a­tion. This the­ory states there are dif­fer­ent selec­tion pres­sures on our genes, depend­ing on which par­ent they came from.

To explain, in a poly­androus mat­ing sys­tem one female mates with mul­tiple males. While both par­ents want their off­spring to have the best chance to sur­vive, the female knows all of the off­spring are hers, while the male can­not be cer­tain which are his. It fol­lows that the genes inher­ited from the moth­er may be selec­ted to favour equal resource dis­tri­bu­tion amongst her off­spring, increas­ing the chances that they all sur­vive and pass on her genes. Where­as genes com­ing from the fath­er may be selec­ted to favour indi­vidu­al resource gain at the expense of sib­lings who may have genes from a dif­fer­ent fath­er. This would increase the chances of the indi­vidu­al sur­viv­ing and passing on the father’s genes to the next gen­er­a­tion. So you can see how genes from the moth­er and fath­er in this scen­ario ‘want’ dif­fer­ent things.

In spe­cies where females mate with mul­tiple males, a female can be cer­tain of their par­ent­age, where­as a male rarely can.

Bumble­bees as an inde­pend­ent test.

This the­ory is based on obser­va­tions in mam­mals. It has been sug­ges­ted social insects could act as an inde­pend­ent test for the kin­ship the­ory of gen­om­ic imprint­ing. This is because, like humans, social insects have many dif­fer­ent social inter­ac­tions with fam­ily-mem­bers. For example, a bumble­bee colony con­sists of a single queen, who has mated with only one male, along with many daugh­ters, who become the work­ers. Bumble­bee colon­ies usu­ally only last for a few months and towards the end of the colony cycle, the queen will start to pro­duce sons and new queens. Some of her work­er daugh­ters (but not all) will rebel against her by becom­ing repro­duct­ive (Fig­ure 4) and pro­du­cing sons of their own, dur­ing what is known as the com­pet­i­tion phase. This is con­sidered ‘treas­on’ and the queen will attack any daugh­ters she sees doing this.

Bumble­bee colon­ies con­sist of a single queen and many daugh­ters (work­ers). Top: inside a colony. Bot­tom: (left) a juven­ile bumble­bee; (centre) the repro­duct­ive ovary of a ‘rebel’ work­er com­pet­ing to pro­duce sons of her own; (right) the non-repro­duct­ive ovary of a stand­ard worker.

Anoth­er reas­on it is believed the kin­ship the­ory applies to bees is because males are genet­ic­ally a little weird. In the world of the bumble­bee, males have a grand­fath­er but no fath­er! Males are cre­ated when queens or work­ers pro­duce eggs that con­tain half of their own DNA, so no addi­tion­al copy of DNA from a fath­er is needed. This means if a work­er pro­duces a son of her own then some of her father’s DNA is likely to be passed on. How­ever, if a queen pro­duces a son, then none of the worker’s father’s DNA will go into that son.

Inher­it­ance pat­terns in bumblebees.

The kin­ship the­ory pre­dicts work­ers rebel and become repro­duct­ive because this would be bene­fi­cial to their father’s genes. Imprint­ing of cer­tain genes would allow a father’s copy to increase work­er repro­duct­ive beha­viour and would also allow a mother’s copy to decrease work­er repro­duct­ive beha­viour. This con­flict is sim­il­ar to the one in the poly­androus mat­ing sys­tem we dis­cussed earli­er. The kin­ship the­ory makes many pre­dic­tions on how imprin­ted genes should work in bumble­bees; work­er repro­duct­ive beha­viour is just one example.

In our cur­rent paper in Evol­u­tion Let­ters, we have iden­ti­fied genes which show par­ent-of-ori­gin expres­sion in a spe­cies of bumble­bee provid­ing sup­port for the kin­ship the­ory. Under­stand­ing how imprint­ing has evolved will facil­it­ate new lines of research into imprint­ing-based dis­eases in humans, such as Beck­with-Wie­der­mann syn­drome. Addi­tion­ally, learn­ing more about non-genet­ic mech­an­isms of inher­it­ance in bumble­bees may one day aid con­ser­va­tion efforts.

Authors: Dr Hol­lie Mar­shall is a Postdoc­tor­al Research Asso­ci­ate at the Uni­ver­sity of Edin­burgh. Dr Eamonn Mal­lon is Asso­ci­ate Dean of Research for the Col­lege of Life Sci­ences and Asso­ci­ate Pro­fess­or of Evol­u­tion­ary Bio­logy at the Uni­ver­sity of Leicester. 

The ori­gin­al art­icle is freely avail­able to read and down­load from Evol­u­tion Letters.