The Evolution of Parental Care Chapter 12 Alcock (Animal Behavior) Tom Wenseleers

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The Evolution of Parental CareChapter 12
Alcock (Animal Behavior)Tom Wenseleers

• Ethology Behavioural Ecology

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Plan of lecture

• Costs and benefits of parental care
• Parent-offspring conflict
• Maternal, paternal biparental care
• Parental favoritism siblicide

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1. Costs and benefitsof parental care
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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 caregivers
  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.

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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 parents working
  harder to supply food) comes at a cost though as
  it may reduce the parents prospects of surviving
  over the winter.
• This effect has been documented in many studies
  in which brood sizes of parents were increased.

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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 parents 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.

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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.
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2. Parent-offspring conflict
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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
  offsprings 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.

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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.
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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.
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Test effect of relatednesson begging loudness

• Begging calls are louder in species with lower
  chick-chick relatedness and this results in more
  frequent predation.

abcde
1 2
3 4
6 7
Species pair
8 9
10 11
-40
-30
-20
-10
Volume of begging calls (dB)
brown headed cowbird
Lower relatedness results in louder calls
Black high relatedness (monogamous)Red low
relatedness (frequent extrapair copulations or
socially parasitic)
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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.

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Siblicide
Spadefoot toads Sand tiger
sharks Piglets
Masked booby
Kittiwake gulls Indian
rosewood
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3. Maternal, paternal biparental care
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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.

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Maternal care Membracinae
treehoppers (boomcicade)
3 independent origins of female parental care
(egg guarding), none of male parental care
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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.

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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.

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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 isless
(mouth brooder)
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Paternal Care male water bugs

• Male water bugs guard and moisten eggs above the
  water(Lethocerus) or carry eggson back (Abedus,
  Belostoma).
• Abedus eggs do not developunless 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.

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3. Intra- and interspecificbrood parasitism
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Discriminating Parental Care

• Misdirecting parental care towards non- offspring
  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.

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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).

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Discriminating Parental Care
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.
Fig 12.9
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Adoption gulls

• Obviously, it would appear beneficial to avoid
  adopting other individuals 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?

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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.

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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 ones 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.
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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 hosts egg
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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.
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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.

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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 hostsparasitized
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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.

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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 hosts young.

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Brood parasitism

• The advantage of laying in the nests of smaller
  species has been shown in experiments in which
  nestlings of non-parasitic 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.

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Why tolerate parasites eggs?

• Given the heavy costs of rearing a parasite, why
  dont 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.

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Why tolerate parasites eggs?

• Accepting a parasites 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
  females territory.

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RenestingNo renesting
12.18
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Why tolerate parasites 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.

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Why tolerate parasites eggs?

• Another reason for hosts to tolerate parasite
  eggs is that the parasite may monitor the nest
  and harm the hosts 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.

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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.

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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.

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Arms race between hosts and parasites

• With many other species the arms-race between
  parasites and hosts is ongoing.
• Horsfields 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.

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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 chicks ability to
  fool the fairy-wren parents is its ability to
  mimic the begging call of young fairy-wrens.

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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.

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(No Transcript)
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4. Parental favoritismand siblicide
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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.

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Young great egrets fight while their
parent ignores the behavior.
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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.
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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

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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.

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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?

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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.

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Parental favoritism and siblicide

• Why do parents play favorites and facilitate
  siblicide?
• There are two major reasons
• Insurance against failure
• Environmental uncertainty

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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).

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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.

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Trade-offs

• Why dont 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 dont 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.

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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.

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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.

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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.

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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.

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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.

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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.

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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.

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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.

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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.
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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.

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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.
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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.