APS 209 Animal Behaviour

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APS 209 Animal Behaviour
Francis L. W. Ratnieks Laboratory of Apiculture
Social Insects
Department of Animal Plant Sciences University
of Sheffield
Lecture 3 The Development of Behaviour A Focus
on Heredity
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Aims Objectives
Aims 1. To show that genes affect behaviour, and
what it means for a gene to affect behaviour. 2.
To show this in several ways (e.g., study of
heritability in natural populations, breeding
experiments) 3. To address some how and why
questions about genes and behaviour. Objectives 1
. To learn specific examples for the above 2. To
understand what it means for a gene to affect
behaviour
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Genotype Phenotype
Genotype The genetic constitution of an
individual. Depending on context, this may refer
to the alleles at a single locus or to the
complete set of genes. Phenotype Any measurable
trait of an individual. Phenotype results from
an interaction between genotype and
environment. Individuals differ as a result of
different genotypes interacting with different
environments. Genetically identical individuals
have identical genotypes, but their phenotype
will differ to a greater or lesser extent. Two
individuals of the same genotype will not have
the same phenotype.
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Nature v Nurture
The role of genes versus environment has been
referred to as Nature versus Nurture. It used
to be controversial that behavioural differences
could be caused by genes. Nature and nurture
would be a fair way of describing the actual
situation. Almost all phenotypic variation,
including behavioural variation, is caused by
several factors. Nature versus nurture is
especially controversial in humans. The human as
a Blank Slate. Human nature can be moulded by
political will or education. Give me the child
and I will give you the man. Ridley, M. 2003.
Nature via nurture genes, experience and what
makes us human. Fourth Estate, London.
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Evolution by Natural Selection
For natural selection to cause evolutionary
change in a behaviour, or any other trait,
requires Heritable variation That at least some
of the phenotypic variation among individuals
within a population is caused by genetic
differences among individuals Differences in
survival/reproduction Individuals with different
phenotypes vary in their ability to survive and
reproduce
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Mouse Nesting
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Mouse Nesting
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Mouse Nesting
Artificial selection on mice over many
generations can increase or decrease bedding
collection for nest construction, in the same way
that many generations of artificial selection can
increase the of oil in maize seed. Results
shows the existence of genetic variation for a
trait.
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Twin Studies
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Nature v Nurture Twin Studies
Identical (monozygotic twins) Non-identical,
fraternal (dizygotic twins) Identical twins
reared together same genes (relatedness of
1.0) same environment Identical twins reared
apart sane genes (relatedness of 1.0) different
environment Fraternal twins reared
together half genes the same (relatedness
0.5) same environment Fraternal twins reared
apart half genes the same (relatedness
0.5) different environment
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Nature v Nurture Twin Studies
Jack Yufe raised by Jewish father in Caribbean
Oskar Stohr raised by catholic grandmother in
Nazi Germany
If we had identical twins reared apart could we
separate the effects on phenotype of genotype and
environment. In some cases this has happened.
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Nature v Nurture Twin Studies
Both like sweet liqueurs Store rubber bands on
their wrists Read magazines from back to
front Dip buttered toast in their coffee Have
very similar personalities
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IQ in Humans
The predicted correlation assumes that phenotypic
difference is only due to genes. The actual
differences are generally lower indicating that
environmental effects are important. The relative
effect of genes and environment can be gauged by
comparisons such as MZ twins reared together or
apart, and parent with genetic or adoptive
offspring. The fact that there is a correlation
between parent and adoptive offspring indicates
an environmental effect. But it may also be
because adoption agencies match the adoptive
parents with the natural parents.
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Verbal Ability in Humans
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Spatial Ability in Humans
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Heritability
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Heritability
The proportion of phenotypic variation in a
population that is due to genetic variation among
individuals that can be inherited. The challenge
is to exclude effects due to common
environment. Heritability can be determined by
comparing the phenotypes of relatives, including
between parent and offspring, and between
siblings (both half and full siblings). Paternal
half siblings can be used to measure
heritability. If a male is mated to several
females the offspring by the different mothers
will be relatives (paternal half siblings) who do
not have the same maternal environment as they
have different mothers. Thus, any phenotypic
similarities of paternal half siblings are due to
the genes they inherited from their father.
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Heritability
5
Heritability 1
Heritability 0.5
4
Mean phenotype of offspring
3
Heritability 0
2
1
1
2
3
4
5
Mean phenotype of parents
The graph above shows how to understand
heritability. In a population individuals vary in
some trait. The trait is measured in offspring
and in their parents (average of the two
parents). If there is no correlation between
parents and offspring heritability is zero. If
the slope of the regression offspring on parents
is 1 then heritability is one etc. The more
heritable the trait the more similar are parents
with offspring.
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Heritability
5
Heritability 1
4
Mean phenotype of offspring
3
Heritability 0
2
1
1
2
3
4
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Phenotype of father
In this example, the trait can only be measured
in one parent. For example, it is a trait found
only in males. Each male is mated to a female who
is randomly chosen from the population. If the
slope of the regression offspring on father is
0.5 then heritability is one. This is because the
father only contributes half the genes of each
offspring. In the previous example we considered
both parents, who together contribute 100 of the
genes of each offspring.
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Migration in Blackcap Warblers
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Migration in Blackcap Warblers
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British Blackcaps
Pre-1950s No Blackcaps in Britain during winter
Birds breeding in Britain migrate to Africa
for winter Birds may also migrate to Africa via
Britain Post-1950s Blackcaps in Britain during
winter Why the change in Behaviour? Britain is
becoming milder and therefore more suitable for
overwintering. British people provide food for
birds.
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Are There Genetic Changes?

• Do genetic differences underlie the changes in
  migration?
• If they do then winter in Britain birds should
  have offspring which inherit this behaviour.
• Research by P. Berthold
• Capture wild British blackcaps in winter
• Transport to laboratory in Germany
• Keep indoors in aviary
• Breed birds in spring in outdoor aviary
• Measure migratory behaviour in offspring
• Note offspring have never migrated before

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Quantifying Migratory Behaviour
Funnel cage. Bird can see night sky but cannot
get out. Bird makes marks on paper on inside of
funnel to show which way it has been trying to
fly.
It is possible to measure the both the tendency
of the blackcaps to migrate (nocturnal migratory
restlessness), and also the direction that they
try to migrate. They use the stars to navigate.
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Quantifying Migratory Behaviour
The offspring of birds caught in the winter in
Britain try to fly west, the same as their
parents. (By contrast, young from birds caught in
southern Germany fly south west.) The similarity
of offspring to parents can only have been due to
genetic similarities.
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Bird Ringing Studies
Canary Islands
Ringing studies eventually showed the migration
routes used. The British summer blackcaps fly
south for the winter, and the British winter
blackcaps are those that have flown in from the
central Germany, Belgium area. Most blackcaps
living on the Canary islands, in the Atlantic off
the coast of Morocco, do not migrate.
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Migration of Hybrid Offspring
Parents from Austria
Parents from S. Germany
F1 hybrid offspring of Austrian and S. German
parents
Blackcaps migrate to Africa from Europe via
Spain, flying southwest, or via the Balkans,
flying southeast. F1 offspring of parents flying
in one or other of these directions, from
southern Germany and Austria respectively, had
intermediate migratory directions. This is
further evidence for the effect of genes on
migratory behaviour.
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Migration in Blackcap Warblers Special Readings
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Heritability of Migratory Activity
This study shows that there is a significant
relationship between the phenotype of the
offspring with the average of their two parents
in terms of nocturnal migratory activity. The
heritability is the slope of this regression, as
the mean of the two parents is used as the
predictor. Berthold, B., Pulido, F. 1994.
Heritability of migratory activity in a natural
bird population. Proceedings of the Royal Society
of London, B. 257 311-315.
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Selective Change in Migratory Activity
This figure shows the extent that migratory
activity would reduce over a number of
generations given a heritability of 0.41 and
selection intensities shown. 80 means that the
birds with the highest 20 migratory activity do
not breed (are selected against). The figure
shows that the population can respond rapidly to
changing environmental conditions requiring less
migration. Berthold Pulido 1994.
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Genetic Basis Migratory Activity
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8
6
Number of half hour periods of migratory
restlessness per night
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2
0
Migratory restlessness, half hour periods per
night, of migratory birds from Canary Islands and
Southern Germany and their hybrid progeny per day
since start of restlessness (x-axis). (Note most
Canary Island birds were non-migratory.)
Berthold, P., Querner, U. 1981. Genetic basis of
migratory behavior in European warblers. Science
212 77-79.
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Migration in Geese Cranes
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Migrating Geese
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Operation Migration Whooping Cranes
Whooping crane Re-establishing migration route
Wisconsin to Florida 13 Dec 2005. 19 birds reach
Florida, guided by 4 microlites a 1100 mile
journey taking 61 days Where to fly is not in
these birds genes!
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Rover and Sitter Behaviour in Drosophila Larvae
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Single Gene Effects Drosophila Larvae
Rover larvae move further when foraging
Sitter larvae move little when foraging
Tracks in petri dish
Cross sitter males with rover females
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Single Gene Effects Drosophila Larvae
F1 generation Virtually all rovers
F2 generation Breed the F1 rovers with each
other to give rovers sitters in 31 ratio
The 31 ratio in the F2 is as expected if
behavioural difference is caused by a single
dominant gene. Further analysis revealed that
just 1 (of the 13061) gene(s) caused the
phenotypic difference in behaviour. (Read the
details and reference from Chapter 3 for further
information.)
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Forager Gene in Honey Bee Workers
The rover gene is also found in the honey bee,
where it is called for, forager. It is present in
all workers, but is only active in forager age
bees. In some way it helps the brain to prepare
for foraging. Robinson, G. E. 2002. Genomics and
integrative analyses of division of labour in
honeybee colonies. American Naturalist 160
S160-S172
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Different Populations of Garter Snakes in
California
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Garter Snake
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Diet of California Garter Snakes
Found in N. America California Moist coastal
areas Drier inland elevated areas Diet of
California garter snakes Coastal feast on
banana slugs Inland eat other things (fish,
frogs etc)
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Banana Slug
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Diet Preferences
Are these behavioural differences (diet
preferences) genetic? Or do snakes just eat what
is available? Test newborn, naïve, snakes with
swab of food.
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Diet Preferences of Newborn Snakes
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Tongue Flicking Behaviour
Tongue flicking on presentation of slug extract
of snakes
Tongue flicks per minute
Read Chapter for more details, including the
all-important controls used.
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General Points
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Take Home Messages
What specific points do the examples in the
lecture and in the book chapter make about
heredity and behaviour? Some are listed below.
Mouse nesting The existence of heritable
variation for a behavioural trait Twin
studies Partitioning behavioural variation into
genetic and environmental components
Heritability The degree to which observed
phenotypic variation in a trait among members of
a population can be passed on from parents to
offspring heritability determines response to
selection. Blackcap migration Showing that a
recent change in behaviour is due at a proximate
level to changes in genes, and at an ultimate
level by changes in environment. (Britain is now
a better place to overwinter, and so some German
blackcaps now overwinter in Britain.) Drosophila
larvae Showing that the exact genetic basis for
behavioural variation can in principle be
determined. The honey bee example shows how gene
expression is linked with the development of the
individual and its behaviour. Garter
snakes Showing that different behaviours are
adaptive in different areas, leading to natural
selection favouring different genes.