Transcript Chapter 12 Alcock (Animal Behavior)

Ethology &
Behavioural Ecology
The Evolution of
Parental Care
Chapter 12 Alcock (Animal Behavior)
Tom Wenseleers
Plan of lecture
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Costs and benefits of parental care
Parent-offspring conflict
Maternal, paternal & biparental care
Parental favoritism & siblicide
1. Costs and benefits
of parental care
Evolution of parental care
• Many species (e.g. clams, barnacles, many fish): NO parental care
Eggs are shed into the water and abandoned. Similarly, turtle young
are on their own once they hatch.
• Decision to offer parental care depends on whether such care will
increase the caregiver’s lifetime reproductive success.
• Greater investment in individual young necessarily reduces the
number of young that can be produced.
• Consequently, species choose between producing many, small,
uncared for young or fewer, larger, cared for young.
• Whales and humans represent one end of the continuum and
barnacles and clams the other.
• If parental care enhances survival and growth of young enough to
compensate for the reduction in young produced then we would
expect parental care to evolve.
Costs and benefits of parental care
• Constraint of parental care: ability of parent to affect offspring
survival.
• Barnacles produce many thousands of eggs which are shed into the
water and drift away. They develop into larvae and one day settle
permanently on a fixed substrate. Barnacles are sessile and can do
nothing to actively assist their young. Not surprisingly, barnacles
have not evolved parental care.
• Parental care in organisms that can give it may significantly enhance
the prospects of the offspring surviving to adulthood. For example,
higher bodyweight at fledging significantly increases a small bird's
chances of surviving to adulthood.
• Extra investment (i.e. the parent’s working harder to supply food)
comes at a cost though as it may reduce the parent’s prospects of
surviving over the winter.
• This effect has been documented in many studies in which brood
sizes of parents were increased.
Costs and benefits of parental care
• In general, the willingness of a parent to invest in or take risk for an
offspring should be influenced by (i) the parent’s future prospects of
reproducing and (ii) the relative value of the current offspring.
• This is borne out by studies of the behavior of long-lived versus
short-lived birds.
• In general, one would predict that long-lived birds should be less
willing to risk their lives to protect their young, but that short-lived
birds should be more willing to do so.
• In general, North American birds are shorter lived than comparable
South American species.
• Ghalambor and Martin (2001) compared the behavior of matched
pairs of North and South American birds to evaluate the birds’
willingness to take risks on behalf of their young.
Fig 12.1A
E.g. Am. Robin (roodborstlijster,
short lived) vs. Arg. Rufous-bellied Thrush (roodbuiklijster,
long lived).
When researchers played tapes of Jays (which raid nests, vlaamse gaai) near the birds’ nests
(B) both species avoided returning to the nest, but robins reduced their activity more,
meaning they were less willing to risk the current offspring.
When a stuffed Sharp-shinned Hawk (a predator of adults) was placed near the nest and
calls played (C), again both species avoided visiting the nest, but this time the Rufous-bellied
Thrushes reduced their visits more, meaning they were less willing to risk their lives by
feeding the current brood.
Hence selection has fine-tuned behavior to take account of costs and benefits of risk-taking
behavior.
2. Parent-offspring conflict
Parent-offspring conflict
• In many species parents invest huge quantities of resources in their
offspring. Initially, both parent and offspring agree that investment in
the offspring is worthwhile because it enhances the offspring’s
prospects of survival and reproduction.
• However, a parent shares only 50% of its genes with the offspring
and is equally related to all of its offspring, whereas the offspring is
100% related to itself, but only shares 50% of genes with full-siblings
(and less with half-siblings) (see Hamilton's IF theory)
• Robert Trivers predicted that this should lead to parent-offspring
conflict over the amount of food provisioned to young. At some point,
a parent will prefer to reserve investment for future offspring rather
than investing in the current one, while the current offspring will
disagree.
Parent-offspring conflict
period of
weaning conflict
Figure shows B/C benefit to cost ratio of investing in the current offspring. Benefit is measured in
benefit to current offspring and cost is measured in reduction in future offspring.
Parent-offspring conflict leads to a period of conflict called weaning during which the offspring tries
to acquire resources and the parent attempts to withhold them.
The period of weaning conflict ends when both offspring and parent agree that future investment by
the parent would be better directed at future offspring rather than to the current offspring. For full
siblings, this is when the benefit to cost ratio drops below ½.
Parent-offspring conflict
period of
weaning conflict
In instances where parents produce only half siblings, we should expect weaning conflict
to last longer, until the B/C ratio drops to 1/4, because the current offspring is less
closely related to future offspring. This has been confirmed in various field studies.
Test: effect of relatedness
on begging loudness
Begging calls are louder in species with lower chick-chick relatedness and this
results in more frequent predation.
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)
Siblicide
• Other possible consequence of young only
being related by 1/2 (full-siblings) or 1/4
(half-siblings): siblicide
• Process whereby some young kill brothers
or sisters.
Siblicide
Spadefoot toads
Masked booby
Sand tiger sharks
Kittiwake gulls
Piglets
Indian rosewood
3. Maternal, paternal
& biparental care
Maternal parental care
• Maternal parental care is more common than paternal care.
• In some instances maternal care is a result of internal fertilization
and the delay between mating and birth (gestation).
• Other general reasons for maternal care being more common focus
on the relative costs to the two sexes of being the caregiver.
• For males there is uncertainty about paternity, which will reduce the
benefit to cost ratio of engaging in parenting.
• In addition, for males when there are opportunities to mate with
multiple females, males that give up that opportunity to engage in
parental care will pay too high a price.
• Paternal care (either with the female or alone) would be selected for
only when the payoff is sufficient to outweigh the costs.
Maternal care: Membracinae
treehoppers
(boomcicade)
3 independent origins of
female parental care (egg guarding),
none of male parental care
Paternal Care: fishes
• In fish male parental care is quite common.
Many males mouth brood eggs or care for eggs
in nests.
• Costs of parental care in these cases seem to
be lower for males than for females. E.g.
because females prefer males that engage in
parental care or because males can take care of
several egg clutches.
Paternal Care: stickleback
• Male sticklebacks can care for 10
clutches of eggs at once.
• Males grow more slowly when
caring for young, but because males
are territorial and cannot range widely
to look for food the additional cost of
parental care is low.
• For a female stickleback parental care would severely
limit her ability to forage and grow.
• Because body size is closely correlated with egg
production loss of foraging opportunities would have a
significant effect on future reproduction.
Paternal Care: fishes
• Because, in many fish, costs of parental care are higher
for females than they are for males, paternal care may
have evolved because males lose less from parental
care than females do. E.g. St. Peter's fish.
difference is
less
(mouth brooder)
Paternal Care: male water bugs
• Male water bugs guard and
moisten eggs above the water
(Lethocerus) or carry eggs
on back (Abedus, Belostoma).
• Abedus eggs do not develop
unless aerated by male.
• Because water bugs are
predatory insects (catching fish, frogs and tadpoles) they
are large and consequently their eggs are too. This is
why oxygenation is necessary.
• Why only male care? Male water bugs with one clutch of
eggs sometimes attract a second female. Also costs of
parental care may be disproportionally great for females
in terms of lost fecundity.
3. Intra- and interspecific
brood parasitism
Discriminating Parental Care
• Misdirecting parental care towards nonoffspring obviously would be a costly
mistake for any organism.
• Many animals rear their young in colonies
and there is plenty of opportunity for
confusion. Yet, as predicted, parental care
is usually very discriminating.
Discriminating Parental Care
Fig 12.7
Young Mexican free-tailed bats at a creche containing 4000 pups per square meter.
Females give birth to a single pup. They use vocal and olfactory cues to identify their
offspring from among thousands in the creche. The bats do occasionally make mistakes
but the benefits of leaving a baby in a creche (mainly thermoregulatory) appear to
outweigh the cost (accuracy from allozyme data: 80%).
Discriminating Parental Care
Fig 12.9
Cliff Swallows often nest in
large colonies and their
young produce much more
variable calls than do Barn
Swallows, which generally
nest solitarily.
Cliff Swallow parents are
also much better at
distinguishing between
calls than are Barn
Swallows.
Adoption: gulls
• Obviously, it would appear beneficial to avoid adopting other
individual’s offspring, but such adoptions sometimes happen.
• In colonially nesting gulls chicks that have been poorly fed in
their own nests sometimes leave their natal nest and join
another brood, where they often are adopted.
• Moving is often a good decision for the chick because it may
end up being better cared for in a different nest.
• However, adoptive parents on average lose 0.5 young of their
own as a result of the adoption so why do they tolerate the
intruder?
Adoption: gulls
• Most likely explanation is that parents use an imperfect
behavioral when deciding who to feed.
• Any chick that begs confidently is accepted and fed. The
reason that they do not discriminate more is probably that
recognition errors would be too costly.
• Errors in which a gull fails to feed or worse attacks and kills its
own chick because it thinks it is a stranger would be very
costly.
• The cost of occasional adoptions appears to be low enough
that selection has not favored higher levels of discrimination in
gulls.
Adoption: goldeneye duck
In some instances adoption may be beneficial to the adopter.
E.g. in ducks it is common for females to accept extra eggs laid in their nests
and to accept stray ducklings into their broods. This may increased the odds
that one’s own young would be saved from predators by the dilution effect. Also,
there is little or no cost to adoption because chicks forage for themselves.
Brood parasitism
• There are several species of
birds that are obligate
interspecific brood parasites.
• These include Old World
Cuckoos (koekoek), Old World
Honeyguides (honingspeurder)
and New World Cowbirds
(koevogel).
• These birds lay their eggs in the
nests of other birds and provide
no parental care.
European Cuckoo removing host’s egg
Brood parasitism
Brood parasitism
appears to have evolved
independently three
times in the cuckoos
and a large number of
cuckoos (53 of 136
species) are brood
parasites.
Obligate brood parasites
indicated in blue.
Occasional parasites
in red.
Brood parasitism
• Interspecific brood parasitism is believed to have
originated as intraspecific brood parasitism.
• Intraspecific brood parasitism is common in birds and
has been recorded in more than 200 species.
• A plausible transition to interspecific brood parasitism
would be for birds to begin laying eggs in the nests of
closely related species.
• Today cuckoos concentrate on species that are not
closely related to them, but as parasitism in cuckoos
may be 60 million years old this may simply reflect the
long period of evolution that has occurred since the
origin of the behavior.
Brood parasitism
• In cowbirds, which much more recently evolved brood parasitism (in
past 3-4 million years) the living species believed most like the
ancestral parasite parasitizes only one other species and that
belongs to its own genus.
• Since then increasingly general brood parasitism appears to have
evolved.
nr. of hosts
parasitized
Brood parasitism
• Brood parasites have a significant effect
on the reproductive success of the hosts.
• Baby cuckoos eject the eggs and young of
the host so the host rears no young of its
own.
Brood parasitism
• Brood parasites exploit the host
parents' tendency to feed the
largest young in a brood and the
one that can reach highest most.
• By laying in the nests of smaller
birds, cuckoos give their young an
advantage in the competition for
food. So do cowbirds whose eggs
hatch after a shorter incubation
period which allows them to hatch
before the host’s young.
Brood parasitism
• The advantage of laying in the
nests of smaller species has
been shown in experiments in
which nestlings of nonparasitic Great Tits and Blue
Tits were switched between
nests.
• The smaller Blue Tits did badly
in Great Tit nests, but Great
Tits prospered in Blue Tit
nests.
Why tolerate parasite’s eggs?
• Given the heavy costs of rearing a parasite, why
don’t hosts reject parasitic eggs? Rejection also
comes with costs!
• Some birds do recognize parasitic eggs and remove
them from the nest. However, there is a risk that the
host will discard one or more of its own eggs in
error.
• Reed Warblers have been shown to make this
mistake.
Why tolerate parasite’s eggs?
• Accepting a parasite’s egg is even more likely to be
adaptive when the host is too small to remove the
parasitic egg.
• Such hosts must either accept the egg or abandon
the nest, which is an expensive option, especially if
nest sites are scarce (e.g. as in cavity nesters).
• Consistent with this hypothesis, Prothonotary
Warblers (citroenzanger) parasitized by cowbirds
are much more likely to abandon their nest and
renest if there are alternative nest sites on the
female’s territory.
Renesting
No renesting
12.18
Why tolerate parasite’s eggs?
• Similarly, Yellow Warblers (gele zanger)
parasitized near the end of the breeding
season tend to accept parasitic eggs,
presumably because there is too little time
to start over.
Why tolerate parasite’s eggs?
• Another reason for hosts to tolerate parasite eggs is that
the parasite may monitor the nest and harm the host’s
nest if the cuckoo's egg was found to be removed.
• This “Mafia hypothesis” has been supported by studies
of Great Spotted Cuckoos and their Magpie (ekster)
hosts.
• Magpie nests from which cuckoo eggs were ejected
suffered a much higher rate of predation (87%) than
nests that accepted cuckoo eggs (12%).
• Threatening the clutch of the hosts appears to be an
effective strategy because renesting is costly in the
magpies’ seasonal environment.
Arms race between hosts and
parasites
• As selection operates on both hosts and parasites
the differing selection pressures have resulted in an
arms race between hosts and parasites.
• In the case of the European cuckoo and its hosts
selection has led to extremely good mimicry of host
eggs.
• Individual cuckoos specialize on one host species
and lay eggs that closely mimic only that species’
eggs.
Arms race between hosts and
parasites
• Historical interactions between cuckoos and some
hosts appear to have resulted in victory for the host.
• E.g., European blackbirds (merel) are rarely
parasitized by cuckoos and even though under no
current selection pressure, these birds reject
parasitic eggs at a very high frequency.
• Apparently, blackbirds evolved rejection behavior in
the past and cuckoos have moved on to other host
species.
Arms race between hosts and
parasites
• With many other species the arms-race between
parasites and hosts is ongoing.
• Horsfield’s Bronze-cuckoo parasitizes the Superb
Fairy Wren (ornaatelfje).
• Fairy-wrens respond to cuckoo eggs laid before they
have started laying by abandoning nest or building
over the egg. They also abandon if cuckoo lays egg
after incubation has begun.
• Bronze-cuckoos have responded by inserting eggs
during fairy-wren laying period. Such eggs are
generally accepted and incubated.
Arms race between hosts and
parasites
• However, when young cuckoo pushes young wrens
out of nest, fairy-wrens abandon the nest about 40%
of the time and cuckoo starves.
• In other cases cuckoo appears to fool parents into
believing their sole chick is a fairy-wren.
• An important factor in the chick’s ability to fool the
fairy-wren parents is its ability to mimic the begging
call of young fairy-wrens.
Arms race between hosts and
parasites
• Another example of the use of calls in the arms
race between parasites and hosts is that of calls
by European Cuckoo chicks in Reed Warbler
nests.
• The rate at which cuckoos call simulates that of
a whole brood of Reed Warblers which
encourages parents to feed at a much higher
rate than they otherwise would.
4. Parental favoritism
and siblicide
Parental favoritism and siblicide
• Parents may be related to all of their offspring
equally, but often do not treat them equally well.
• In many cases parents actively discriminate against
certain offspring and either allow them to starve or
allow their siblings to kill them.
• For example, in African Black Eagles the first
hatched of two chicks attacks its younger sibling as
soon as it hatches and pecks it to death.
• Similarly in egrets (reiger), boobies (gent), pelicans
and other birds older siblings attack and drive
younger offspring out of the nest where they starve
to death.
Young great egrets
fight while their parent
ignores the behavior.
At a Brown Booby (bruine gent)
nest the older chick (under its
parent) has driven its smaller
sibling from the nest where it will
die of exposure and starvation.
Parental disciplining
• Siblicide is sometimes countered
by parental disciplining.
• E.g. blue-footed booby
(blauwvoetgent) parents prevent
their young from killing each other
• On the other hand, the masked
booby (gemaskerde gent) allows
chicks to kill each other
Parental favoritism and siblicide
• Sometimes parents seem not only to tolerate
siblicide, but to actively encourage it.
• For example, in Black Eagles incubation begins
as soon as the first egg is laid.
• As a result the first egg hatches 3-7 days before
the second and so the older offspring has a
huge size advantage over its younger sibling
and can easily kill him.
Parental favoritism and siblicide
• Such hatching asynchrony is very common
among birds and results in an age and size
hierarchy within the brood.
• Birds do not have to hatch their young
asynchronously and many birds (e.g. ducks),
even though they lay large clutches, hatch their
young synchronously. So why do they do it?
Parental favoritism and siblicide
• In cattle egrets (and other birds) in addition to
promoting hatching asynchrony, parents spike
the earlier laid eggs with high doses of
androgens (male hormones).
• The hormones make the earliest hatched chicks
more aggressive and gives them an extra
advantage over later hatched chicks.
Parental favoritism and siblicide
• Why do parents play favorites and
facilitate siblicide?
• There are two major reasons:
– Insurance against failure
– Environmental uncertainty
Insurance
• The most extreme form of brood reduction
is obligate brood reduction in which
younger offspring essentially always die.
• Examples of obligate brood reducers
include: Black Eagles, Harpy Eagles
(harpij), Giant Pandas, and Hooded
Grebes (Patagonische fuut).
Insurance
• These animals have no intention of rearing more than a single
offspring.
• The second offspring represents an easily cancelled
insurance policy against the failure of the first offspring to
hatch or develop normally.
• When the first offspring arrives it kills its sibling (Black Eagle),
the parents cover over the second egg (Harpy Eagles), the
parents abandon the second egg (Hooded Grebes) or
abandon the second born cub (Giant Pandas).
• Thus, the parents avoid prolonged investment in a back-up
offspring. However, if the first offspring fails the second can
step in and take its place.
Trade-offs
• Why don’t these animals go ahead and rear the
second baby once it arrives?
• In many cases parents would appear to be capable
of rearing two young, but don’t do so. Why not?
• Because there are trade-offs between offspring
number and quality as well as between offspring
number and parental future reproductive success.
Trade-offs
• For these species it is usually not possible to
provide enough food to rear two high-quality young.
Pandas feed on low quality food and the burden of
providing milk for two cubs is too much for most
mothers. Two weakling offspring are worse than a
single sturdy cub.
• In addition, extra effort invested in trying to rear two
young in a season generally reduces future
reproductive success by reducing lifespan and
ability to produce eggs or babies.
Environmental uncertainty
• Many other species are facultative brood reducers which
means that brood reduction does not always occur.
• These species practice a policy of parental optimism.
• They lay a clutch size that can be reared in a good year,
but in a bad year will result in brood reduction.
• In these species the brood contains two classes of
offspring: core and marginal offspring.
• Marginal offspring are handicapped by the parents and
as in obligate brood reducers have insurance value, but
mainly are produced so that parents can take advantage
of a good year if one occurs to rear bonus offspring.
Environmental uncertainty
• Consistent with this idea, in facultative brood reducers,
the handicap the parents create is enough to create a
clear hierarchy in the brood but not so great that it
cannot be overcome.
• Thus, in cattle egret broods the effects of A and B chicks
(the eldest chicks) aggression towards younger C and D
chicks is moderated by food supply.
• If food is plentiful, the younger chicks can tolerate the
beating and may survive to fledge. If food is scarce the
younger chicks quickly starve or are driven out of the
nest and die.
Environmental uncertainty
• The cattle egret parents’ policy of hatching asynchrony
thus creates a situation in which in good years conditions
can be taken advantage of and extra babies reared, but
in bad years the brood can be efficiently reduced to what
foraging conditions will support.
• The amount of asynchrony in cattle egret broods
appears to have been tailored by natural selection to
maximize parents reproductive success and efficiency in
rearing babies.
Environmental uncertainty
• Artificially synchronized nests produced fewer survivors and
required more food because offspring fought more and so expended
more energy.
• Nests in which asynchrony was exaggerated produced similar
numbers of young as normally asynchronous nests, but brood
reduction took place at younger ages, which may limit the ability of
the parents to rear large broods in good years.
Brood reduction and humans
• Discussions of brood reduction are applicable to humans
also. Twin births are rare, but twin conceptions are much
commoner and only one in ten to one in fifty twin
conceptions produce twins. The other pregnancies result
only in singleton births. This phenomenon has been
dubbed the “vanishing twin” syndrome.
• Part of the phenomenon may be that producing extra
eggs is an insurance strategy against pregnancy failure
due to defective embryos. Some of these early embryos
have chromosomal defects and are quietly aborted by
the mother.
• Indeed, older women are more likely to give birth to twins
than younger women, they polyovulate more frequently
and chromosomal defects are more common.
Evaluating the reproductive
value of offspring
• As we have seen not all offspring are
created equal and even in the absence of
parental manipulation of quality we would
expect parents to assess offspring quality
when deciding how to allocate scarce
resources.
Evaluating the reproductive
value of offspring
• It has been suggested that the
gape color of baby birds may
signal the quality of their immune
system and thus offspring quality
• Red gape color is produced by
carotenoid pigments in the blood
and these are believed to
enhance immune function.
Evaluating the reproductive
value of offspring
In an experiment on barn
swallows in which chicks
gapes were colored with
food coloring chicks whose
gapes were reddened
received more food, while
chicks whose gapes were
yellowed did not.
Evaluating the reproductive
value of offspring
• Alternative explanations for the role of gape
coloration have been put forward, however.
• An obvious alternative is that parents are not
assessing offspring quality, but just feeding those
chicks whose gapes are more conspicuous under
the prevailing lighting conditions.
• Consistent with this idea Great Tit chicks whose
mouths were painted yellow received more food
than chicks whose mouths were painted red and
were less conspicuous in a dark nest box.
• When a perspex lid was placed on the nest box
however, both sets of chicks were fed equally.
Evaluating the reproductive
value of offspring
Coots (meerkoet) reduce brood sizes by pecking
certain babies in their brood when they beg for food
and these ones quickly die.
Baby coots have prominent long orange tipped
plumes on their backs and throats and these may
be a cue parents use in deciding which chicks they
wish to feed.
When these plumes were trimmed from half the
members of a brood the unaltered members of the
brood received more food and grew faster than the
trimmed birds (black). (C,E)
Control broods in which all birds were trimmed
survived as well as broods in which no chicks were
trimmed. (B,D)
Coots thus appeared to discriminate against
trimmed chicks because they lacked orange plumes
not because they could not recognize them.
Thus, it may be that the orange plumes are a signal
of offspring quality.
Magpie assessment of
offspring value
Magpie (ekster) young are
increasingly likely to survive
as they age. Thus their value
increases and one would
expect parents to value them
more.
Consistent with this parents
are more likely to engage in
defensive behavior when a
predator approaches a nest if
the brood is older.