Transcript Practicals (19.5h) Exercises (13h)

Ethology &
Behavioural Ecology
The Evolution of Communication
Chapter 9 Alcock (Animal Behavior) p. 282-313
p. 275-281: not for exam
Tom Wenseleers
Communication
• Definition: the transfer of information from
signaler to receiver
• Two evolutionary puzzles:
– How can signals evolve?
– What mechanisms can maintain signal
honesty and prevent deception?
1. The evolutionary
origin of signals
Problem
• For an effective signal to evolve an animal
not only needs to acquire the ability to
produce the signal but others also need to
be able to detect and respond to such
signals
• How can this ever evolve?
Male whistling moths
Male whistling moths use ultrasound produced by modified forewings ("castanets")
to communicate.
Some related ancestors are preyed upon
by bats, and in response these moths
evolved the perceptory machinery to hear
bat-produced ultrasound waves.
So perceptual machinery was in place and
this may have led to the evolution of a
special organ to produce ultrasound for
communicative purposes.
(they themselves do not have bat
predators)
Co-option of an ancestral signal
In most or all bowerbirds (tuiniervogels) males use the "skraa" call to
threaten rivals. In one cluster of closely related species, this signal now
also serves a courtship role.
Sensory exploitation & biases
Sensory exploitation: when signal givers tap into preexisting perceptual
mechanism; leads to sensory biases. Example: courtship by male water
mites. (A) Female is in prey-catching position. The male approaches
and waves a trembling foreleg in front of her, setting up water vribations
similar to those a copepod might make. Female may respond by
grabbing him, but releases him unharmed. (B) The male then deposits
spermatophores in front of the female.
Preexisting sensory biases
Male and female guppies eat Clusia fruits which are orange due to
the presence of carotenoids. The same carotenoids also accumulate
in males and lead to colourful patterns.
Observation: females prefer colourful, bright red males.
Why? Preexisting sensory bias for detecting orange fruits.
Preexisting sensory biases
Mate preferences for a novel
male ornament: in long-tailed
finches and zebra finches
females prefer white crested
males. Why? Perhaps because
they line their nest with white
feathers.
2. The maintenance of
signal honesty
What mechanisms favour honest communication?
J. Maynard Smith & B. Harper (2003) Animal Signals. Oxf Univ Press.
3 ways that signals may be honest/reliable:
1. Common interest
dance language in honeybees: incl. fitness benefits
communication within a body
raven yelling: mutualistic benefits
plant-insect communication: mutualistic benefits
2. Handicap/cost
begging by bird chicks
male displays used to attract females
3. Index of quality (uncheatable signals)
loudness and depth of calls by males
body size
Signal honesty due to common interest
Example
Signaller
Receiver
What is the benefit of
producing the signal?
What is the benefit of acting
on the signal?
Communication Your head
Increase survival of
within your
organism and help the
body
transmission of copies of
the gene(s) responsible for
the signal
Your leg
Increase survival of
organism and help the
transmission of copies of the
gene(s) responsible for
signal reception
Dancing bee
Dance following bee
Honeybee
colony productivity Increase colony productivity
dance language Increase
and the bee’s inclusive
and the bee’s inclusive
fitness.
fitness.
Raven
communication
Yelling raven
Other ravens
Increase chances of
establishing a territory.
Being guided to food.
Plant-insect
communication
Plant
Insect
Signal nectar availability
and get pollinated.
Obtain more food (nectar).
Honest communication
due to common interest
Example: insect societies
Waggle dance
Dance followers
(unemployed foragers)
"Receiver"
Karl von Frisch: 1973: Nobel Prize
Dancer (forager)
"Signaller"
Angle of waggle run correlates with angle of food source relative to the sun;
duration of waggle run correlates with distance of food source; total number of
waggle runs correlates with the quality of the food source
Tremble dance
• performed by returning foragers with
nectar who experience long unloading
delays to receiver bees
• consists of irregular movements in all
directions
• recruits more nectar receiver bees and
also reduces the amount of foraging
Alarm pheromone
Produced by Koschevnikov gland, near sting shaft
Consists of more than 40 chemical compounds, including isopentyl acetate (IPA)
Communication in leaf-cutting ants
fungus garden
pheromone trail
Leaf-cutting ants stridulate to recruit
other cutters and minims, which protect the
leaf-carrying ants against parasitoids and help
maintain pheromone trails
hitchhiking minims
Queen egg marking
• In honeybees workers can lay eggs but such
eggs are eaten by other workers
("worker policing")
• Workers benefit from policing because they
are more related to the sons of the queen
(r=0.25) than to the sons of other workers,
many of which are half-nephews (r=0.125)
(honeybee queens mate with ca. 10 males)
Ratnieks & Visscher Nature 1989
Queen egg marking
• Workers can tell worker-laid from queen-laid
eggs because the queen marks her eggs with
a pheromone
• The queen (signaller) benefits from producing
the signal because it protects her eggs
• The workers (receivers) benefit from it
because they will end up rearing the more
closely related male offspring of the queen
Dishonest communication
due to divergent interests in
insect societies
Anarchistic bees
• Rare lineages of anarchistic bees:
workers lay eggs that mimic the smell of
queen-laid eggs
• Such eggs are not policed
• Usually displayed by workers from one
particular patriline
• Benefits the rare workers that produce such
deceptive signals because they end up
producing sons (r=0.5) or full-sisters' sons
(r=0.375) rather than brothers (r=0.25)
Oldroyd et al. Nature 1994
Communication honesty in
insect societies
• Common interests are strong
– Individuals are related to each other
– Food collected by different workers feeds the same,
related brood
– Usually leads to honest/reliable communication
• But conflicts can occur
– Can lead to deception in communication
– Particularly over reproduction
– Relatedness of 1 would eliminate all potential for
conflict
(e.g. cell-cell relatedness in multicellular organism)
Honest communication due to
common interest among
nonrelatives: raven yelling
Benefits of raven yelling
• Background
Large mammal carcasses are rare. But can be valuable
resource to Maine ravens in winter. One carcass could
provide months of food.
• Observation
Many ravens were seen feeding on a dead moose.
• Puzzle
Ravens are rare
Would need to call ravens from other groups
Would not be relatives
• Question
What is the benefit of communicating (yelling)?
Hypotheses for adaptive significance
Attract a "carcass opener" such as a bear
(and incidentally more ravens)
Against
Against
Lone ravens finding a carcass did not yell
Ravens at an opened carcass sometimes did yell
Selfish herding: attract more ravens in case of attack
Against
Yelling continued at carcasses with many ravens
Overwhelm defence of territory holding ravens
For
For
For
For
For
Territory holding ravens did not yell
Non resident ravens did yell
Yelling attracted other ravens to a carcass
Territory holders unable to repel many non residents
Carcasses eaten by 1 or 2, or by many ravens
Raven yelling
Communication or non-communication are both favoured by
common interests. Territory holders are better off if they don't
yell, in order to monopolise a carcass. Non-residents are
better off if they yell, in order to attract others to defend the
carcass against residents.
Honest communication
due to common interest in
interspecific interactions
Example: plant-insect communication
Nectar guides
• nectar guides: guides insects to
nectar
• plant gets pollinated at same time
• horse chestnut: nectar guide is
yellow when it produces nectar;
when flower stops producing nectar it turns red
• both parties benefit: plant gets pollinated more
effectively, insect can collect more nectar
• since it signals the timing, not the amount of
nectar secreted, there is no incentive for the
plant to provide deceptive signals
Honest communication due
to costs: begging in chicks
Begging chicks & feeding parents
• Why do chicks beg?
• Background
Parents often give more food to chicks that beg more.
Begging can attract predators.
• How can begging be an honest signal of need?
Evolutionary argument: cost-benefit.
• Testing cost-benefit predictions
Effect of relatedness (extra-pair parentage)
• Exploitation of parents by begging
Brood parasites
Why feed chicks who beg more?
Parents feed begging chicks more
Pied flycatcher
(bonte vliegenvanger)
Pied flycatcher birds. Only one parent heard a taped begging call at the nest.
The other heard no call. The parent who heard the call, whether male or
female, responded by bringing back more food. Thus, on the left the female
brings back more food when she hears begging (upper inverted triangle) than
when she does not (lower triangle).
Costs of begging: nest predation
Begging is also costly. There is the cost of
making the calls, but more importantly it
increases net predation. The cost to the chick
is losing its own life, but also losing the lives of
siblings (Hamilton's rule).
In this study artificial nests were more likely to
be predated if begging calls (from two species)
were played. The black-throated blue warbler
("blauwe zwartkeelzanger") is a tree nester,
and the ovenbird ("ovenvogel") a ground
nester. The begging calls of tree nesters attract
more predators. But predation risk in trees is
lower than on the ground, so tree nesters beg
more loudly.
Adaptation in warbler begging calls
Chicks of ground-nesters which are more prone to predation produce higher-pitched
begging calls, and high-frequency sounds do not travel as far.
How can begging be an honest signal?
A. How can begging by chicks be an
honest signal of need for food?
B. Why don't chicks beg
maximally whatever their need?
If a chick that begs more gets more food (A) and if more food
increases survival, why don't chicks then beg at the maximum
intensity (B)? But if they do this, then there should be no
correlation between begging intensity and need for food (B). As
we will see, if there is a cost to begging this can lead to begging
intensity being correlated with the need for for food (A).
Costs to chick from begging more
The more the chick begs the greater the predation risk to the nest. The
effect is probably linear or close to it. Thus, if the chick begs for 60
minutes not 30 minutes it will double the chance of attracting a predator.
Benefits to chick from begging more
The more the chick begs the more food it is given by its parents. But the
curve shows decreasing returns as each additional increment of food is
worth less to it in terms of increased survival.
Benefits to chick from begging more
The optimum begging intensity for chick 1 is where the difference
between cost and benefit are greatest.
Benefits to chick from begging more
Now we consider a second chick who is less in need of food. For chick
2, the extra food obtained by any level of begging is worth less to it in
terms of increased survival than for the hungry chick. So chick 2's
optimum level of begging is less. As a result, there is a correlation
between hunger level and begging intensity.
Benefits to chick from begging more
In this example, we can see that lowered
predation risk, such as from tree nesting,
results in higher optimum levels of begging.
But the optimum level of the hungry chick is
still more than for the less hungry chick.
Begging & relatedness
Also inclusive fitness costs due to increased predation of siblings.
Results in louder optimal begging calls in species with
lower chick-chick relatedness.
1 Hirunda rustica
a
2 Tachycineta bicolor
a
b
4 Prunella modularis
5 Passerina cyanea
6 Melospiza melodia
c
7 Zonotrichia leucophrys
d
8 Calcarius lapponicus
Species pair
3 Sialia sialis
1
2
b
c
3
6
4
7
d
8
9
e
10
11
9 C. pictus
e
10 Agelaius phoeniceus
11 Molothrus ater
brown headed cowbird
-40
-30
-20
-10
Volume of begging calls (dB)
Lower relatedness results in louder calls
Black: high relatedness (monogamous)
Red: low relatedness (frequent extrapair copulations or socially parasitic)
Honest communication due to costs:
revealing handicaps in males
Signalling quality with a costly display
This imaginary example considers the costs and benefits to a male of
making a large display. The display is attracting to females (double mating
success) but reduces survival. The survival cost is greater to low quality
males. So only high quality males benefits (survival x matings) from making
a display. The display is an honest signal of quality, a handicap that only
high quality males can afford.
Amotz Zahavi
Human example of a
Zahavian handicap
conspicuous consumption
Conspicuous consumption is a trait not easily faked, and is an honest
indicator of those who possesses resources.
Honest communication due to
uncheatable indices of quality:
body size
Toad calls
Toad calls
Male toads with a female were gagged so that they could not call. Taped
calls were then provided at either low or high frequency. Low frequency
calls deterred rival males more than high frequency calls. In general, larger
toads make deeper calls. Small toads cannot easily make deep calls.
Therefore, deep calls are an honest signal of male size and likely ability to
deter a rival.
Cheating body size
possible up to a point
inflating abdomen
puffing out chest
making hair stand on end
elongating larynx to make
deeper calls
Honest signals are expensive
In the side-blotched lizard, males
that have run on a threadmill to
lower their endurance are not able
to maintain their threat posture for
as long, and generate fewer pushup
displays.
Honest signal in antler flies
Antler fly males confront each other
head-to-head.
The head projections are large,
elaborate & expensive to produce.
Antler span and eye span are
closely correlated with body size.
Honest signals in red deer
Only red deer stags in top condition can roar for long periods.
Deceptive communication
between species
Brood parasites: cuckoo
Cuckoos are brood parasites. One cuckoo chick displaces an entire
brood of reed warbler chicks. The begging intensity of one cuckoo chick
(D) is similar to an entire brood of reed warbler chicks (C) and much
greater than a single reed warbler chick (B).
Brood parasites: cuckoo
The begging of one cuckoo
chick is as effective at
causing the reed warbler
parents to feed it as the
begging of an entire brood
of warbler chicks.
Brood parasites: cuckoo
• Why does the reed warbler listen to the
cuckoo signal?
• Of course it would be selected to try to
detect cuckoos and not feed those chicks
• But this may be costly since the erroneous
underfeeding or rejection of an own chick
would greatly reduce the warbler's fitness
Sexual deception
• Mimicking female to attract and eat male
Fire fly femme fatale (Note: fire flies are beetles, not flies)
Bolas spider
• Why is a male attracted?
Males are still attracted because, on average, following the
signal will increase his fitness because mimics are
relatively rare. Even a single mating with a female will
bring high fitness.
Deception: fire fly femme fatale
Male Photinus fireflies are
attracted to species-specific
flashing of female. Another
predatory firefly (Photuris)
mimics this, and the amorous
male is killed.
Deception: bolas spider
The bolas spider attracts moths by
mimicking the female moth's pheromone.
Only male moths of one or two species are
caught. The moth is caught on a sticky line
that the spider swings in a circle beneath
it. Ignoring the female sex pheromone
would impose a large cost.
Deception: anglerfish
Anglerfish have a lure that
looks like a small prey item
to smaller fish. It then preys
on these smaller fish.
Again, the smaller fish will
always be selected to
respond to such visual
stimuli because not doing so
would lead to starvation.
Signal exploitation
by other species
Origin of the honeybee
dance language
• bumblebees: use scent to mark
the location of food sources
• more derived honeybees and
stingless bees: use dances or
sounds to communicate the
location of food sources
• hypothesis: strategy to avoid
other species or other unrelated
colonies from evesdropping on
scent-marked food sources?
Illegitimate receivers
Females of the tungara frog prefer males that give whining calls with chucks (blue in
sonogram). However, males that emit such calls are more likely to be preyed upon by
fringe-lipped bats.
Avoiding signal exploitation
"Seet" call of the great tit:
alarm call used when a
flying sparrow hawk is
seen
(koolmees)
(sperwer)
Is a high frequency call
that is not easily heard by
sparrow hawks; also does
not travel large distances.
Convergent evolution of "seet" call