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APS 209 Animal Behaviour. Lecture 4. The Development of Behaviour: A Focus on Environment. 1. Non-adaptive responses to the environment 2. Adaptive responses to the environment: different environments giving different behaviours, behavioural/morphological strategies, learning

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APS 209 Animal Behaviour

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APS 209 Animal Behaviour

Lecture 4. The Development of Behaviour:

A Focus on Environment

1. Non-adaptive responses to the environment

2. Adaptive responses to the environment: different environments giving different behaviours, behavioural/morphological strategies, learning

3. Buffering against environmental challenges: different environments giving same behaviour

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Aims & Objectives


1. Show how behaviour can be flexibly adjusted according to environmental conditions; behavioural “switches”.

2. Show how behavioural development can overcome some disruptive environmental effects (isolation, lack of food).


1. Learn examples of the above

2. Understand the adaptive significance (i.e., the ultimate benefit in terms of survival/reproduction/passing on copies of your genes) of the variety of ways that an organism’s behaviour responds to environmental conditions.

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Foetal Environment & Adult Behaviour

Mice have litters of offspring

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Foetal Environment & Adult Behaviour

In many mammals, foetuses develop in litters within the uterus. During foetal development, the brain is also developing. This is influenced by hormones produced by the foetus. However, the hormones produced by one foetus may affect nearby foetuses.

Frederick von Saal et al. delivered mice by caesarean section. This allowed them to document their position in the uterus and the sex of their neighbours.

The young males were castrated and later in life were given testosterone implants. This ensured that any differences between adult males were not due to differences in testosterone following birth.

Measured behaviour of males and females with 0, 1, 2 male neighbours: 0M, 1M and 2M.

Each individual had one of three types of uterine environment. By comparing 0M, 1M and 2M mice the researchers could test the hypothesis that uterine environment affects subsequent behaviour.

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Foetal Environment & Male Aggression

The effect of foetal environment on male behaviour. (A) The level of estradiol, is greater around male foetuses who are between 2 female embryos (0M) than between 2 male embryos (2M). This probably has an effect on brain development: adult 2M males are more aggressive (B).

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Foetal Environment & Female Home Range

There were also effects on females. 2M females are behaviourally masculinised and have larger home ranges than 0M females. They are also less sexually attractive.

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Foetal Environment & Adult Behaviour

The study clearly shows that the foetal environment affects adult behaviour in mice.

You may be looking for an adaptive reason. But probably there is none. The fact that mice have litters of offspring and that hormones leak out of an individual foetus and affect neighbours is probably an inevitable consequence of the way mouse reproduction and development occurs.

Presumably, the effects are not so great as to cause great harm. If not, we might expect natural selection to result in less harm.

The foetal mice are close relatives, and would be selected not to harm each other greatly. We will go into the interests of siblings in a later lecture in the section on mathematical insights.

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Adaptive Responses to the Environment: Honey Bee Foraging

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Honey Bee Foraging

Apis mellifera on borage, Borago officianalis. Drawing by former APS 209 student Lila Morris.

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Age and Work in Honey Bee Workers

Cleaning cells

Feeding larvae

Feeding nestmates

Packing pollen


Age of bee, days

In a normal honey bee colony, the queen is laying eggs every day and this results in the adult worker bees being all ages, with young adult workers emerging every day. The workers do different jobs (division of labour) according to their age. The oldest workers are foragers.

How is this age-dependent change in behaviour regulated?

How can it respond to environmental conditions, such as in a colony with an unusual distribution of workers ages?

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The Role of Juvenile Hormone

  • Juvenile Hormone (JH) is an important insect hormone. It is secreted by a gland in the head called the corpora allata (CA). It regulates development at moulting, that is whether the next instar is an adult or not. In worker bees, which are adult insects, it regulates their ageing and the tasks they perform.

  • Age-related behavioural transitions regulated by JH changes

  • Robinson, G. E. et al.

  • Young bees (e.g. nurses): have low JH levels

  • Old bees (e.g. foragers): high high JH levels

  • Treat young bees with JH →→ precocious foragers

  • Remove CA →→ delay onset of foraging behaviour

  • Remove CA and administer JH →→ foraging

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Developmental Changes in Worker Bees

Forager bees have different brain morphology. The Kenyon cells of the mushroom bodies decrease in size. Fibres of the mushroom bodies increase in size

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Developmental Changes in Worker Bees

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What Stimulates Bee to Become Forager?

Results from an experiment in which hives of only young worker bees were set up. These young bees did not forage when older workers were added to their colony (left). But they did forage when younger workers were added (right). This shows that the age at which a worker starts to forage is flexible and responds to the age structure of workers in the colony. This is important as during swarming or following replacement of the queen, there is a break in the rearing of workers.

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Primer Pheromone

Nectar receiver

Nectar forager

Worker Apis mellifera nectar forager (right) transferring nectar to a receiver bee in hive. Drawing by former APS 209 student Lila Morris.

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Primer Pheromone

The regulation of foraging in honey bee colonies is complex and not fully understood. Recently, it was discovered that forager bees produce a pheromone in their crop (stomach), where the nectar is held while foraging before transfer to a receiver. The presence of this pheromone in the colony tends to inhibit younger bees from becoming foragers.

Leoncini, I. et al 2004. Regulation of behavioral maturation by a primer pheromone produced by adult worker honey bees. Proceedings National Academy of Sciences USA 101: 17559-17564.

Abstract: Previous research showed that the presence of older workerscauses a delayed onset of foraging in younger individuals inhoney bee colonies, but a specific worker inhibitory factorhad not yet been identified. Here, we report on the identificationof a substance produced by adult forager honey bees, ethyl oleate,that acts as a chemical inhibitory factor to delay age at onsetof foraging. Ethyl oleate is synthesized de novo and is presentin highest concentrations in the bee's crop. These results suggestthat worker behavioral maturation is modulated via trophallaxis,a form of food exchange that also serves as a prominent communicationchannel in insect societies. Our findings provide critical validationfor a model of self-organization explaining how bees are ableto respond to fragmentary information with actions that areappropriate to the state of the whole colony.

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Queen & Worker Caste in Honey Bee

Environment 1

Food: royal jelly

Female larva

Environment 2

Food: not royal jelly

Honey bees have two morphologically and behaviourally distinct female castes: queen and worker. Every female larva has the potential to develop into either by switching on the correct set of genes. The larva only develops into a queen if it is in the right environment to do so: a cell filled with special food known as royal jelly. The larva responds adaptively to its environment. A larva in a worker cell that tried to develop into a queen would have insufficient space and food to do so.

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Adaptive Responses to the Environment: Amphibian Larvae

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Cannibalistic Larvae: Tiger Salamander

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Cannibalistic Larvae: Tiger Salamander

  • Tiger salamander larvae come in two morphologically and behaviourally different forms. Both are aquatic but differ especially in their head morphology.

  • Normal: eats small pond invertebrates

  • Cannibal: larger head & jaws, will eat ‘normal’ larvae

  • Cannibals develop:

  • At higher density of salamander larvae

  • When individuals differ greatly in size

  • When individuals develop with largely non-relatives

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Cannibalism & Kinship

These data show that cannibal morphs are less likely to develop when the other salamanders are kin. From a “why” perspective this is because killing relatives has a cost due to kin selection/inclusive fitness. We will examine this in greater detail in the lecture on mathematical insights. From a “how” perspective it shows that they have some way of recognizing kin. Pfennig has found a similar situation in larval spadefoot toads, with two morphs one of which is more predatory and can be cannibalistic. In the spadefoots, a larva is more likely to develop into the predatory morph if it eats shrimp larvae.

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W. D. Hamilton

Hamilton, W. D. 1964. The genetical evolution of social behaviour. Journal of Theoretical Biology 7: 1-52.

Inclusive Fitness Theory

“The social behaviour of a species evolves in such a way that in each distinct behaviour-evoking situation the individual will seem to value his neighbours’ fitness against his own according to the coefficients of relationship appropriate to that situation.”

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Cannibalistic Spadefoot Toad Tadpole

A spadefoot toad tadpole consuming a smaller member of its own species. Cannibalistic individuals tend to avoid eating their kin. Some of the questions I am currently investigating include: How and why are such discriminations achieved? Why are some families consistently better than others at identifying their kin? Are cannibals at heightened risk of disease? (photo © Thomas A. Wiewandt, DRK)”

Text from D. Pfennig


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Adaptive Tadpole Morphs

“Spadefoot tadpoles often occur in nature as either a small-headed omnivore morph (upper tadpole in upperphoto), which develops slowly and feeds mostly on algae and detritus, or as a large-headed carnivore morph (lower tadpole), which develops rapidly and feeds on animal prey. Spadefoots are born as omnivores, but if a young tadpole ingests anostracan fairy shrimp (lower photo), it may develop into a carnivore. What evolutionary forces maintain such different phenotypes in the same population? How are alternative phenotypes produced from a single genotype?” (upper photo © David Pfennig; lower photo © David Sanders)

Text from D. Pfennig


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Male Anthias: sex change fish

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Mechanical Vibrations in Environment Cause Salamander Larvae to Become Carnivores

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Effect of Shortening Prey Tadpole Tails

Larvae were kept with tadpoles of one of the two prey species above. The proportion that developed into the big-headed morph (carnivores) was lower when the tadpoles had 2/3 of their tails surgically removed.

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Effect of Shortening Prey Tadpole Tails

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Effect of Stirring the Water Mechanically

Larvae were kept individually in small containers that were either stirred, n = 10, or not, n = 10 (controls). Stirring was 10Hz for 1.5 seconds with a 20 second break then another 1.5 seconds of stirring etc.

The proportion of larvae that developed into the big-headed morph was greater when stirred, 60% (6/10), than when not stirred, 0% (0/10). P = 0.01.

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Effect of Stirring the Water Mechanically

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The researchers studied larvae of the salamander Hynobius retardatus. This species has a small headed morph and a broad-headed carnivorous morph that preys on tadpoles and even larvae of its own species. They found that development of the carnivorous morph was stimulated by vibrations in the water that could be caused by tadpoles of two species of anurans (toads and frogs) or even by a mechanical stirring device. Thus, in this species of salamander, the larvae adaptively respond to their environment by sensing something as simple as the agitation of the water caused by potential prey.

Michimae, H., Nishimura, K., Wakahara, M. 2005. Mechanical vibrations from tadpoles’ flapping tails transform salamander’s carnivorous morphology. Biology Letters 1: 75-77.

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Kin Recognition

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Belding’s Ground Squirrel

Diurnal social rodent

High-altitude meadows of western USA

Hibernates during winter, emerges May

3-6 pups per year

Males disperse, females stay in natal area

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Belding’s Ground Squirrel

New born offspring switched to produce 4 classes

Siblings reared apart

Siblings reared together

Non-siblings reared apart

Non-siblings reared together

Juveniles are reared, weaned and then put in an arena together

Interactions were observed

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Belding’s Ground Squirrel

Animals reared together “treated each other nicely” regardless of whether they were true siblings or foster siblings. Animals reared apart likely to be aggressive to each other.

This shows that animals probably learn who their kin are by associating with them as young.

But biological sisters reared apart were less aggressive to each other than non-siblings reared apart.

This shows that there is some ability to recognize kin directly by genetic similarity.

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Belding’s Ground Squirrel

Aggression of siblings reared apart versus non-siblings reared apart.

Sisters show less aggression to each other than to unrelated females.

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Phenotype Matching

Wherever kin recognition occurs there must be some underlying mechanism.

It is possible to recognize kin by comparing a conspecific to some template representing kin. The template is probably learned and may be the odour of yourself, or that of your nest, or the individuals that you were reared with.

That female Belding’s ground squirrels can recognize their full sisters even when they have not been reared with them indicates the use of some part of the phenotype with a genetic underpinning. That is, kin share genes and this results in a more similar phenotype.

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Kin recognition. Polistes wasps

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Kin recognition. Polistes wasps

Overwintered female wasps start building nests in the spring. Two females often nest together, with one helping the other and doing little reproduction. The two wasps are usually nestmates, who were reared in the same nest the previous summer. They can recognize each other by odours on their cuticle that they have acquired from their nest.

Honey bee colonies, and colonies of most social insects, have entrance guards. The guards prevent intruders, including conspecifics from different colonies, from entering the nest. In most species, the guards have to learn a template representing the odour of their own colony.

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The animal learns something about its environment, such as where food is.

Learning leads to changes in the brain. These changes may be detectable morphologically, such as by the enlargement of part of the brain.

Learning is often made in specific contexts, and an animal has the ability to learn things relevant to these contexts. Thus, rats have the ability to associate a food odour with later nausea, and thereby can learn to avoid certain foods that are inedible or poisonous. But rats cannot associate a sound with later nausea.

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Learning and Brain Changes in Tits

Coal tit

Marsh tit

Black capped chickadee

Mountain chickadee

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Learning in Black Capped Chickadee


Birds in aviary: artificial “trees” with 72 velcro covered holes

Birds store 4-5 sunflower seeds

Birds removed from aviary, seeds removed

Birds returned to aviary

Birds spend more time picking at covers on holes where seeds had been previously stored

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Learning and Brain Changes in Tits

Hippocampus is involved in spatial learning

Telencephalon is not involved in spatial learning

In tits, the size of part of the brain, the hippocampus, was larger in birds that had stored food versus control birds that had not.

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Taxi Drivers’ Brains

Taxi drivers’ brains are not like other people’s. The posterior hippocampus of London cabbies is larger than that of non-taxi drivers. The more years of driving, the bigger it gets. As in the tits, performing a behaviour involving learning locations (taxi driving) causes neurological changes which in turn make the animal (the cabbie) better at the behaviour

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Avoidance Learning, Thynnine Wasps

Orchid flower resembles female wasp

Male wasp copulating flower

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Avoidance Learning, Thynnine Wasps

Place orchid in a jar in new location and count visits by male wasps

Male thynnine wasps are deceived by orchids that mimic the odour of female wasps. The males attempt to copulate with the orchids and thereby transmit orchid pollen. However, wasps learn to avoid odour from locations which they have visited only to find orchids not females. They do not learn to avoid the odour, because this would mean that they did not respond to female wasps. But they learn to avoid the location.

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Aversive Learning in Rats

not easily learned

easily learned

easily learned

Rats easily learn to avoid specific flavours associated with nausea. They can also learn associations between sounds and skin pain. This pattern is adaptive. Some foods with specific flavours may be toxic and will later cause nausea. Rats feed carefully. They only take a little of anything new. They can’t clear their digestive tract by vomiting. This study shows that the animal is programmed to learn certain things about its environment. It does not have completely general learning potential.

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Buffering Against the Environment

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Buffering Against the Environment

Dutch people born during famine in WW2 have normal intelligence.

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Take Home Messages

Mouse behaviourThe environment can have major effects on the behaviour of animals, particularly where the effect is caused via development, via long-lasting effects on the brain. Not all environmental influences result in adaptive changes. This effect is probably “noise”.

Honey bee foragingThe animal is usually affected by its environment in an adaptive way. Here the worker bees adjust their behaviour to colony needs. The environment can exert its effect in a multiple ways.

Amphibian larvaeThe animal responds to its environment by altering its development, resulting in coordinated changes in behaviour and morphology. The type of environment may be detected in a variety of ways, with subtle effects such as “crowding” interacting with “kinship” to influence whether or not a cannibal morph is favoured.

Kin recognitionResponding to the social environment, especially the degree to which you are interacting with kin versus non-kin. How does an animal know who its kin are?

LearningLearning can result in a rapid change that makes an animal better suited to its environment. But learning is not completely general. Some things are learned more easily than others.

BufferingIn many cases the animal should not allow the environment to affect its development or behaviour.

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