Transcript No Slide Title

CONFLICT AND COOPERATION
Sex
Parasitism versus Mutualism
Jacobus J. Boomsma
Institute of Biology
University of Copenhagen
Resource Allocation
Cooperation does not come easy
• Who gives alarm calls?
• Can policing and punishment evolve?
• Are policing and punishment necessary for
stable cooperation?
• How important are kinship and reciprocity?
• How special are human societies?
• Reciprocal exploitation and conflicts in
mutualisms
Evolution is essential for all biology
“Nothing in biology
makes sense,
except in the light
of evolution”
(Dobzhansky, 1973)
A Portrait Gallery of Evolutionary Biologists
1800
1850
Source of
inspiration
Darwin
Malthus
Wallace
1900
1950
2000
A Portrait Gallery of Evolutionary Biologists
1800
1850
1900
Source of
inspiration
Darwin
Malthus
Mendel
Wallace
1950
2000
A Portrait Gallery of Evolutionary Biologists
1800
1850
1900
1950
Source of
inspiration
Fisher
Darwin
Malthus
Mendel
Wallace
Wright
Haldane
2000
A Portrait Gallery of Evolutionary Biologists
1800
1850
1900
1950
2000
Source of
inspiration
Fisher
Darwin
Malthus
Dobzhansky
Mendel
Wallace
Haldane
Mayr
Wright
The roots of Behavioral Ecology:
Tinbergen, Hamilton and Williams
Tinbergen (1963)
Survival value
of behaviour
Williams (1966)
The first synthesis
Hamilton (1964)
Evolutionary
roots of social
behaviour
Ecology is essential for understanding
evolution
• “ Nothing in biology makes sense,
except in the light of evolution ”
(Dobzhansky, 1973)
• “ Very little in evolution makes
sense except in the light of
ecology ”
“Ecology provides the stage
on which the “evolutionary
play” is performed”
(Townsend, Harper & Begon,
2000)
Darwinian Ecology
Evolutionary Ecology proper
(animals, plants, micro-organisms)
Behavioural Ecology
(animals)
Sociobiology
(social animals)
Darwinian Ecology
Kin selection:
The only real
Innovation
e.g. Life Histories
after Darwin
Natural selection
and
Sexual selection
Darwinian sexual selection
Female choice
Male-male competition
Darwin’s Problem with Insect Societies
“ I……… will confine myself to one special
difficulty, which at first appeared to me
insuperable, and actually fatal to my whole
theory. I allude to the neuters or sterile
queen
females in insect communities:
for these neuters often differ
widely in instinct and in
structure from both the males and the
fertile females, and yet, from being sterile,
they cannot propagate their kind.”
workers
Darwin (1859) “The Origin of Species”
Hamilton’s Solution
Reproductive “altruism”
evolves when:
br > c
b = benefit (extra offspring of relatives
raised because of helping)
r = relatedness of donor to recipient
c = cost (own offspring not raised due
to helping)
Parent-offspring conflict (Trivers 1974)
• Benefits gradually
decrease per u.o.i.
• Costs stay constant or
increase
• Parents weigh costs and
benefits equally
• Offspring discount
parental costs by their
average relatedness to
future sibs
Parent-offspring conflict (Trivers 1974)
• Young want more PI (y)
than parents are selected
to provide (p)
• y-p is even larger when
current of future sibs
have a different father
(maximize B – C/4)
• Mother equally related to
all offspring
• Offspring related to itself
by r=1
Parent-offspring conflict theory
Parents
Offspring
Dad 1
Mom
Dad 2
R.L. Trivers
Parent-offspring conflict and
sib-rivalry are relatedness-linked
r = 0.5 r = 1.0 r = 0.5 r = 0.25
Genetic relatedness
Reciprocal altruism - The “ prisoner’s dilemma ”
1
2
1
Cooperate
Defect
Defect
Swap?
2
Cooperate
1
2
1
2
1
2
1
2
“Defection” is favoured. Mutual cooperation only pays in repeated exchanges.
“ Nature, red in tooth and claw ”
Tennyson (1850)
• Merciless
• Exploitative
• Fundamentally selfish
• Cooperation in nature
needs to be explained by
individual (gene) level
selection and not by group
selection
“Good for the
species arguments”
Insect colonies as model systems
2 cm
2 cm
Simple ant colony in an acorn
Primitive wasp
colony
From centimeters…...
Large insect colonies
2 cm
Previous slide
…. to meters
2m
Length: ~100 x
Area: ~10 000 x
Mass: ~1 000 000 x
Advanced tropical ant colony
Large colonies are like societies
Tropical honey bee
Tropical wasp
Long-lived
Elaborate nests
Tropical termite
Simple and complex family structures
x
Parents
complex
half-sib family
daughter queen
mates and takes over
x
offspring
x
simple
full-sib family
x
x
Queens are specialized egg-laying
females
Single queen per colony
Multiple queens per colony
Reproduction in haplodiploid social
insects (ants, bees, wasps)
Queen ovaries
worker ovaries
workers
Mother queen
Not mated
No stored sperm
father
no
Fertiliz ation
queen sons
Fert ilization
queen daughters
no
Fertiliz ation
worker sons
Relatedness consequences of
haplodiploidy
Reproductive Conflict over
Sex ratio
and
Male production
Mother queen
workers
0.25
0.25
0.50
0.50
0.75
0.50 (own son)
0.375 (other worker’s son)
father
0.50
0.00
queen son
0.25
worker son
queen daughter
The conflict over Male Production
When there are more half sisters than
full sisters workers are selected to
remove each other’s eggs
workers
Mother queen
0.25
0.25
0.50
0.50
0.75
0.50 (own son)
0.375 (other worker’s son)
father
0.50
0.00
queen son
0.25
worker son
queen daughter
Worker-Queen Conflict in Ants, Bees, Wasps
• Worker control over sex
allocation is common
• Worker production of
males is not
Who wins reproductive conflicts ?
In species with
small colonies
many try to
reproduce but
queens manipulate
reproduction
to their own
advantage
Queens always win in Bumblebees
Who wins reproductive conflicts ?
Workers tend to win sex ratio conflicts
in large ant societies
In species with
large colonies
queens monopolize
reproduction but
workers raise
sisters or brothers
depending on their
own best interests
Nepotism is prevented by worker policing
• Queen eggs are marked
with a queen pheromone
• Worker male eggs
lack this pheromone
• Worker eggs are
recognised by other
workers and removed
• Worker policing is
evolutionary stable in
honey bees
Photos and data: Francis Ratnieks
Cooperation does not come easy
• Who gives alarm calls?
• Can policing and punishment evolve?
• Are policing and punishment necessary for
stable cooperation?
• How important are kinship and reciprocity?
• How special are human societies?
• Reciprocal exploitation and conflicts in
mutualisms
How special are Human Societies?
• We have culture !!!
• But is culture really 100% independent of
genes?
• How relevant is fitness in human societies
and can it be measured?
• Do humans fit inclusive fitness theory?
• If so, what does this imply?
• Cooperation does not come easy
Mutualistic Symbiosis and Co-evolution
nitrogen
binding
bacteria
mycorrhizae
corals
chloroplasts
gut bacteria
Ectosymbionts of Insect Societies
lichens
mitochondria
ants and fungi
termites and fungi
The Conceptual Paradigm
“Many of the benefits sought by living things are
disproportionally available to co-operating groups......
The problem is that while an individual can benefit
from mutual co-operation, each one can also do even
better by exploiting the co-operative efforts of others”.
R. Axelrod and W.D. Hamilton, The evolution of co-operation.
Science 211: 1390-1396 (1981)
When and Why do Symbiotic Partners
Cooperate?
• Exploitation and monopolization of novel
resources
• Sufficient alignment of reproductive interests
to stabilize interactions in spite of potential
conflict
• ....... i.e., to allow Stable Bilateral Exploitation
Agricultural Insect Societies
Attine Ants in Panama
Macrotermitinae in West Africa
Attine ants
Fungus growing
termites
Fieldwork in Panama
Smithsonian Tropical
Research Institute
Panama Canal
Ant fungus-farming started simple
Dead Substrate:
Leaf debris
Wood chips
Insect body parts
Insect frass
Mycocepurus nest
The evolutionary history of fungus-growing ants
Ant Phylogeny:
Schultz & Meier (1995) and
Schultz et al. unpublished
Lower Attines
Fungus
rearing
Mueller et al., 1998
Higher Attines
Special
Clones
Leafcutting
Herbivory
Leafcutters Large Colonies
Ant agriculture became “herbivorous”, ……
One of which
Split into
became
two genera,
really dominant,
……
……
QuickTime™ and a
Cinepak decompressor
are needed to see this picture.
Damaging, ……
Biggggg..
An underground metropolis
which may live for decades
A society with millions of
workers, all daughters of
the same long-lived queen
After Jonkman
highly sophisticated Ants
TheAndLeafcutter
Acromyrmex
Atta
From Hölldobler and Wilson, 1990
castes
gongylidia
anal droplets
How an Atta colony starts
fungus
fragment
Winged queen and male
One year old nest
And What it Finally Becomes
Fungus rearing Assembly Lines
• Evolution towards clonal fungi
• More genetic diversity of ants per
nest via multiple queen mating
• Worker policing phenomena
expected
Ongoing work Mischa Dijkstra
Photo: Mark W. Moffett
Genetic Marker Studies
Microsatellite tandem repeat sequence
# repeats variable
among individuals
Leafcutter Ants Have Highly Harmonious Societies
Villesen, Murakami, Schultz & Boomsma (2002)
Lower Attines
Higher Attines
Large Colonies,
Worker Castes & Live
Substrate associated
with genetic
diversity
Leafcutters
A Symbiosis of at least four parties
From Schultz, 1999
C. Currie
M. Poulsen
Acromyrmex
As Laboratory Model System
Three sympatric species in
Gamboa, Panama:
A. octospinosus
A. echinatior
A. insinuator (inquiline)
Division of labour
Internal
Foragers
Acromyrmex echinatior
Ac. echinatior
Proportion of sample
0.6
0.5
0.4
0.3
0.2
0.1
0
0.6
0.8
1
1.2
1.4
1.6 1.8
2
2.2
2.4
2.6
2.8
Head width (mm)
Data: Bill Hughes
How to cope with
parasites and diseases?
Incompatibility Issues
Acromyrmex
Incompatibility
Incompatibility reaction
3
2
1
0
0
0,05
0,1
0,15
0,2
0,25
0,3
Mean genetic distance
0,35
0,4
0,45
Social parasites: Do not build nests,
but simply move in
Acromyrmex echinatior host
Parasite and host are sister species
Parasites never carry Streptomyces
Picture: Klaus Lechner
“Go to the ant, thou sluggard:
consider her ways, and be wise”
Proverbs 6:6
The world’s
largest and
smallest ant
The discussion program this afternoon
• A recapitulation of social insect conflicts
• An experimental study of policing and
punishment in ants
• Linking social evolution in insects and
vertebrates
• How important is kinship in vertebrates?
The conflict over Male Production
Queen always values own son most (0.5)
Worker always values own son most (0.5)
Workers prefer full sister sons (0.375)
over queen sons (0.25)
Workers prefer queen sons (0.25)
over half sister sons (0.125)
Mother queen
workers
0.25
0.25
0.50
0.50
0.75
0.50 (own son)
0.375 (other worker’s son)
father
0.50
0.00
queen son
0.25
worker son
queen daughter
SPLIT SEX RATIO THEORY
Boomsma & Grafen 1990, 1991
rf = 0.75
rm = 0.25
RA=3
rf = 0.50
rm = 0.25
SINGLE MATING
HIGH RA
MULTIPLE MATING
LOW RA
“SPECIALIZE IN FEMALES”
“SPECIALIZE IN MALES”
RA=ca. 2
Formica truncorum Sex allocation
Number of colonies
Queen singly mated
Queen multiply mated
8
1989
7
6
5
4
3
2
1
0
0 - 0.2
0.2 - 0.4
0.4 - 0.6
0.6 - 0.8
Investment in females
0.8 - 1.0
Who wins reproductive conflicts ?
Males?
Reproductive organs
Formica queen
Formica nest mound
Males posthumously
manipulate worker
reproductive strategies
by clumping sperm
Sperm storage organ
After Hölldobler and Wilson, 1990