Queenworker caste determination and kin conflict over caste fate

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Queen-worker caste determinationand kin
conflict over caste fate

• Carlos Lopez-Vaamonde

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Lecture 5 Aims

• To discuss how differential gene expression
  underlies queen-worker caste determination in the
  social Hymenoptera. This is central to understand
  how variation in gene expression underlies
  adaptive phenotypic variation.
• To set out the basic predictions of kin conflict
  over caste determination for the social
  Hymenoptera.
• To examine whether the predictions of the theory
  are met in nature (i.e. stingless bees).

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Lecture 5 Outline

• Queen-worker caste determination. Alternative
  phenotypes
• Evolution of polyphenisms
• Association between queen-worker caste
  determination and differential gene expression in
  the social Hymenoptera.
• Polistes canadensis (paper wasp)
• Bombus terrestris (bumblebee)
• Apis mellifera (honeybee).
• Kin conflict over caste determination for the
  social Hymenoptera.
• Test of caste determination
• Melipona (stinglessbee).

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Queen-Worker Caste Determination

• The evolution of sterile castes in the social
  insects represents one of the major transitions
  in evolution.

• The worker caste is entirely female and, like
  queen caste, arises from fertilized, diploid eggs.

• Caste determination refers to the process by
  which a totipotent, female individual (capable of
  becoming a member of either caste) develops into
  an adult queen or worker.

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Queens Workers
Queens are morphologically, physiologically and
behaviourally specialized for egg-laying.

• Workers are specialized for helping and either
  lack ovaries or, if they have them, usually lack
  a sperm receptacle and are unable to mate and
  produce haploid offspring.

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Differential expression of genes

• With few exceptions, whether female larvae
  develop into queens or workers depends NOT on
  genetic differences but on their environment at
  critical periods of caste determination.

• Caste determination and differentiation must
  involve the differential expression of genes
  shared by queens and workers.

• Social Hymenoptera present a unique opportunity
  to investigate how variation in gene expression
  underlies adaptive morphological and behavioural
  diversity.

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Complex Castes Systems

• Morphological
• Permanent
• Determined as larva (royal jelly)
• The identity of differentially expressed genes
  associated with queen-worker caste determination
  in larvae has only been investigated in the
  advanced social honeybee Apis mellifera.(Evans
  Wheeler 1999, 2000)
• Genes associated with caste determination in the
  honey bee are irreversibly switched on/off

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Simple Caste Systems

• Morphologically identical
• Behavioural roles
• Flexible, reversible
• Determined during adulthood
• Differential gene expression?

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Evolutionary Origin of Castes

• Complex societies evolve from simple ones

Bumble Bee Pereboom et al. submitted
Honey Bee Evans Wheeler 99
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Important questions

• 1) Are behavioural castes associated with
  differential gene expression?
• 2) How do patterns of expression differ in
  simple and complex castes?

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Finding Genes Subtractive Hybridization
Q
Enrich Normalise
W
CGCTACGGTATTTTTCAGCTTCGTTAACCATTCTCTCAATATCTTCCTTG
CTAAGACGTCCCTTATCGTTGGTAATAGTGATTT
Y
BLAST
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Methods Microarrays
Q
W
Y
Genetic array showing genes expressed
differentially by honeybee workers and queens
during caste determination
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Simple Caste System

• Paper wasp - Polistes canadensis
• Behavioural castes
• Tropical no seasonal constraints
• All young females totipotent

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Ontogeny of P. canadensis
Age
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Results

• 1) Are behavioural castes associated with
  differential gene expression?
• 2) How do patterns of expression differ in
  simple and complex castes?

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Results 1 Shared Expression Levels
(n39 genes)
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Queens and young females in Polistes have
discrete genes, but workers are intermediates
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Expression patterns of individual genes
Some genes are upregulated (showing relatively
higher levels of expression) in queens and some
are downregulated
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Single pathway to queenhood

• Behavioural castes are associated with
  differential gene expression along a single
  pathway to queenhood.

Young
Workers
Queens
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Conclusions 1

• Are behavioural castes associated with
  differential gene expression?
• Yes!
• Single genomic pathway to queenhood
• Workers are genomic intermediates

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• 1) Are behavioural castes associated with
  differential gene expression?
• 2) How do patterns of expression differ in
  simple and complex castes?

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From Simple to Complex Castes
Simple
Paper wasps Sumner et al unpublished

• Single pathway

• Single pathway
• Temporal segregation of gene expression within
  genome

Bumble Bee Pereboom et al. sub

• Caste-specific gene allocation within
• genome
• Distinct queen/worker pathways

Honey Bee Evans Wheeler 99
Complex
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Conclusions gene expression/caste determination

• Social Hymenoptera represent excellent systems to
  investigate how variation in gene expression
  underlies adaptive morphological and behavioural
  diversity.

• Caste evolution associated with
• temporal separation within genome
• caste-specific allocation of genes

• Comparative studies of caste-related gene
  expression provide essential insights into the
  nature, origin and evolution of caste polyphenism
  in social insects.
• But, these are early days!
• Natural History genomics

Single queen-rearing cell
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Why become a worker?
Workers Give up reproduction for the benefit of
their mother queen
Darwinian puzzle The sterile worker caste of
the social Hymenoptera poses one special
difficulty, which at first appeared to me
insuperable, and actually fatal to my whole
theory. Darwin (1859) On the Origin of Species

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Kin conflict over Caste Determination

• benefit of becoming a queen gaining greater
  direct reproduction
• SO WHY DO NOT MANY FEMALES OPT TO BECOME QUEENS?
• females benefit from becoming a queen, BUT colony
  would suffer if all would do so
  caste fate conflict
• individual benefits but collective suffers
  tragedy of the commons

Bourke and Ratnieks 1999. Kin conflict over caste
determination in social Hymenoptera. Behavioural
Ecology and Sociobiology 46 287-297.
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Tragedy of the commons

• Each individual gains by pursuing interests that
  increase returns relative to neighbours but
  decrease the value of the common goods. If all
  succumb to the temptation of free-riding, the
  outcome is a collective disaster. William
  Forster Lloyd 1832

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Overgrazing
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Socially controlled, Caste fate enforced

• In many social insects females are unable to
  choose their own caste since their fate is
  determined by the quantity and quality of the
  food they receive from the adult workers
  nutritional caste determination.
• For instance queen rearing in honeybees (royal
  jelly)

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Exception Melipona stingless bees

• In Melipona stingless bees conditions for actual
  caste conflict are met

• Queens and sexuals are reared simultaneously

• Immature female individuals can potentially
  control their own caste fate because queens and
  workers are similar in size self-determination

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...in fact queens are slightly smaller
Melipona beecheii
mean 57.1 mg
F3,48076.3, p lt 1E-13
mean 48.2 mg
gt66.1 mg
lt26.6 mg
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Develop in cells of uniform size
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Mass-provisioning

• Female larvae have practical power over their own
  nutrition because they are provisioned by workers
  with food and the cell in which they develop is
  then sealed.

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Predictions

• The theory of kin-selected caste conflict
  predicts
• More queens should emerge than are favoured by
  the workers, due to female larvae selfishly
  developing as queens

• It likewise predicts worker actions to correct
  the excess of queens.

These predictions are fulfilled by Melipona
Bourke and Ratnieks 1999. Kin conflict over caste
determination in social Hymenoptera. Behavioural
Ecology and Sociobiology 46 287-297.
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Melipona supports predictionexcess queens
Queen production in Melipona is characterized by
the emergence of a vast excess of queens ( up to
25, of diploid larvae emerge as queens).
A piece of uncapped comb of Melipona subnitida
reveals that queens are produced in excess
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Large-scale cull of queens by workers
A Melipona subnitida queen ecloses from her cell
Immediately afterwards, the workers aggress and
kill the queen.
Finally, the workers dump the dead queen corpse
and leave it to decompose in the colony. The fact
that queens are killed by the workers shows they
are produced in excess.
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Reproduction by fission

• A factor that probably aggravates this phenomenon
  is that stingless bees reproduce by colony
  fission.
• The colony, which in most species is monogynous,
  divides into two, with each new colony headed by
  a young queen produced in the mother colony.

• Therefore only a handful of new queens is
  required for colony reproduction per fission
  event, making the unnecessary excess of queens
  that emerges likely to represent a significant
  cost to the colony.

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What about other social insects?

• other swarming social insects
• Honey bees
• trigonine stingless bees

• Relatively large degree of queen-worker size
  dimorphism
• Queens develop in cells larger than those for
  workers

• caste fate enforced via food control. Lack
  self-determination

• Consistent with this in these species there is no
  large-scale overproduction of queens and hence no
  cull of excess queens.

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Alternative explanations for excess queen
production in Melipona ?
Other explanations

• Insurance against queen loss

• queen overproduction is far too high
• queen replacement takes 10 days (in this period
  up to 70 queens are produced)

• Or a mechanism that allows workers to have a
  stock of queens from which to select the most
  fecund

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Conditions for actual caste conflict

• Small queen-worker dimorphism
• Simultaneous rearing of queens and workers
• Self-determination Developing female larvae have
  some practical control over own nutrition

• Reproduction by colony fission (because excess of
  queens will be costly to colony, and will
  therefore be likely to be culled)

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Summary

• Social insect caste system provides scope for
  conflict
• Social insect females benefit from developing as
  a queen
• Melipona females selfishly exploit colony by
  developing as queens (self determination)

• results in tragedy of the commons queen
  overproduction
• what limits exploitation within the group?

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Costs to kin can limit exploitation

• Exploitation becomes less profitable when
  selfishness causes cost to kin
• Queen overproduction causes depletion of
  workforce and has two costs to kin
• reduced ability to swarm
• reduced production of males
• Prediction less exploitation when group members
  are highly related reduced exploitation.
  Hypothesis never tested

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What can we learn from all this?
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Insight into conflict resolution
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