親代照顧和交配體系 (parental care and mating systems) ─ 動物行為學 (ethology)...

親代照顧和交配體系(Parental Care and Mating Systems)

─ 動物行為學 (Ethology)

鄭先祐 (Ayo)

國立臺南大學環境與生態學院生態科學與技術學系教授

Ayo NUTN Web: http://myweb.nutn.edu.tw/~hycheng/

大學部生態學與保育生物學學程 ( 必選 ) 2010 年秋冬

Ayo 教材 (動物行為學 2010) 2

Part 3. 個體間的互動

生殖行為 (Reproductive Behavior) 親代照顧與交配體系 (Parental Care and Mating

Systems) 溝通：管道與功能 (Communication: Channels and

Functions) 溝通的演化 (The Evolution of Communication) 衝突 (Conflict) 團體生活，利他和合作 (Group Living, Altruism,

and Cooperation)


14 親代照顧和交配體系(Parental Care and Mating Systems)

Parental care Conflicts ( 衝突 ) among family members Some factors that influence the allocation of parental

resources Overall patterns of parental care Dispensing with( 免除 ) parental care– brood

parasitism Mating systems

Classifying mating systems Monogamy ( 一對一 ) Polygyny ( 多妻制 ) Polyandry ( 多夫制 )


Reproduction is a complicated affair

In several species of mammals, including humans, mothers that produce sons incur greater costs than those that produce daughters Higher parasite loads A delay in the next reproductive effort Reduced likelihood of future reproduction Reduced longevity


Sons are expensive

Mothers who produce sons experience reproductive costs Making them less able to invest in their next child

Human offspring born after elder brothers had similar survival But lower lifetime reproductive success than offspring

born after elder sisters due to Lower lifetime fecundity (number of offspring

produced)


In a preindustrial human population in Finland, producing sons does not affect the survival of subsequent offspring but does affect the lifetime reproductive success of subsequent offspring.

(a) the probability of surviving to 15 years of age in relation to the sex of elder offspring.

(b) Lifetime reproductive success, defined as number of children raised to 15 years of age, in relation to the sex of the elder offspring.


Parental care

Parental investment: investment by parents in an offspring That increases the survival of that offspring But decreases the ability of investment in other offspring

Direct parental behaviors Have an immediate impact on offspring and their survival Nursing, feeding, grooming, transporting, huddling with

young Indirect parental behaviors

Are performed while away from the young Do not involve direct physical contact with offspring Still affect offspring survival, but not immediately


Indirect parental care in mammals

Includes acquiring and defending critical resources Building and maintaining nests or dens Defending offspring against predators or infanticidal

conspecifics Caring for pregnant or lactating females is included

Pregnancy and lactation are energetically demanding Delivering food to females is very helpful

Male owl monkeys feed lactating females ( 餵奶的雌性 ) Increases the quantity and/or quality of milk produced Which reduces the interval between births of offspring Parents benefit by producing more, well-fed offspring


Parental investment maximizes reproductive success An individual’s lifetime reproductive success is

maximized Not necessarily each reproductive event

Parents must make two decisions How much of their resources to devote to reproduction

instead of to their own growth and survival How to allocate available resources among their

offspring These decisions can lead to conflicts of interest

Between parents and offspring And among siblings


Conflicts over parental investment: sexual conflict

Sexual conflict: conflict between the evolutionary interests of males and females Particularly mating and parental investment

Involves interactions between males and females during which Each individual’s fitness depends on its own strategy As well as the strategy of its partner

Conflict in parental investment emerges because the costs of providing care are paid separately by each parent Both parents benefit, regardless which one provides the care Each parent prefers that the other do most the work


Conflicts over parental investment: intra/interbrood conflicts

Intrabrood conflict: young try to obtain resources That the parents prefer to distribute to other members

of the current brood Interbrood conflict: young try to obtain resources

that parents prefer to save for future offspring Differences in the distribution of resources by parents

can lead to sibling rivalry ( 競爭 ) Each youngster derives a greater fitness benefit from

the parental care it receives than from the care its siblings receive


Sibling rivalry( 競爭 )

Involves overt, substantial aggression Can result in siblicide: the death of one or more

siblings In other species, rivalry is subtler

Lower levels of fighting Scramble competition: siblings race to outcompete

each other for parental resources, with lower levels of fighting


Sibling competition in domestic piglets

Begins before birth The uterus is too small to support maximum growth of

embryos Some embryos die

Others survive but have low birth weight Are at a severe disadvantage for the intense postnatal

competition Piglets( 小豬 ) compete for teats

Large piglets locate and retain possession of a teat Smaller piglets are displaced and starve


Piglet battles

Battles involve frantic shoving and wounding Newborns have slashing canine( 犬牙 ) and incisor( 門牙 )

teeth That function solely in early sibling competition


Siblicide

Sibling rivalry leads to one offspring attacking and killing its brother or sister

Common in species where resources are limited And parents deposit eggs or young in a “nursery” with

limited space Nursery = a uterus, brood pouch, parent’s back, nest, or

den It may be advantageous to save the parents time and

energy By eliminating the young least likely to reach adulthood


Factors influencing allocation of parental resources: life history

Expected life span influences a parent’s allocation of resources To maximize lifetime reproductive success

Whether parents have future opportunities to breed Is affected by the parent’s age and the life span

In short-lived species with little hope of producing more young Parents invest more heavily in the present young

Parents of long-lived species spend more of their resources on their continued growth and survival Because they might have the opportunity to breed again


Parental care in Leach’s storm-petrel ( 白腰叉尾海燕 )

Storm petrels are long-lived seabirds Adults visit food patches to feed their

chicks Foraging trips last two to three days so the

cost of flight is significant

When parent petrels were handicapped They passed the increased reproductive costs to their offspring And maintained their own nutritional condition Chicks grew more slowly and spent more nights without food


Parental care in starlings ( 椋鳥 ) and tits ( 山雀 )

When reproductive costs of short-lived starlings and tits were increased They bore part of the increased costs themselves They allocated the same amount of resources to their

chicks In short-lived species

Each clutch represents a large part of the parent’s lifetime reproductive success


Factors influencing allocation of parental resources: certainty of paternity

Parental solicitude( 掛念 ) toward young is correlated with the likelihood of genetic relatedness

Females are certain that they are related to their offspring 50% of a mother’s genes are present in each of her progeny

A male cannot be so confident He has no guarantee that his sperm fertilizes her eggs He risk investing time and energy in raising another male’s

offspring, resulting in Decreased chances of evolution of paternal behavior


Certainty of paternity influences parental care in sunfish

Male bluegill sunfish ( 藍鰓太陽魚 ) decrease parental care when they are less certain of their paternity

Parental males compete for nest sites, guard females and care for young Sneaker males steal fertilizations and do not provide parental

care Parental males had chemical cues from fry( 魚苗 ) to

reassess( 評估 ) their paternity


Certainty of paternity influences level of parental care by male bluegill sunfish. (a) In experiment (treatment group) display less parental care toward eggs than males not exposed to sneaker males (control group). (b) males whose clutches had been manipulated (1/3 eggs been exchanged).


Factors influencing allocation of parental resources: gender of offspring

Parental investment is influenced by gender of the offspring

Sex allocation: the manner in which parents distribute resources between sons and daughters

Parents can bias their allocation in two ways They can produce more offspring of one sex They can provide more (or better) resources to offspring of

one sex Most animals divide resources equally between sons and

daughters Others (i.e. brown songlarks) distribute resources unevenly


Songlarks distribute resources unequally

Polygynous warblers: one male mates with more than one female Extreme sexual size dimorphism: males

are twice as heavy Mothers feed the young

At birth, nestling males and females do not differ in body mass But males become much heavier Male nestlings receive more, higher

quality prey


Songlark mothers bias their parental investment toward their sons. (1) although male and female nestlings have similar body masses at hatching, males become increasingly larger than females in the nest few weeks. (b) mother not only deliver prey at higher rates to broods with more males, they feed male nestlings a high quality diet than they feed female nestlings.


The benefit of raising large male offspring

Raising male offspring is costly to the mother Large body size is an important determinant of male

reproductive success Less important for female reproductive success

By producing large sons that will successfully attract and compete for mates Mothers ensure that their genes are well-represented in

future generations


Patterns of parental care

Differences exist among taxa in the extent and pattern of parental care

Within vertebrates: most teleost fishes, frogs, toads, lizards, and snakes show no parental care at all

All crocodilians and mammals display some form of parental care Also typical of most birds

A few species lay their eggs in the nests of others And relinquish all care to the “host” parents


Female-only care

The most common form of care in mammals Internal gestation and lactation necessitate a major

parental role for the female Early paternal care is always in conjunction with

maternal care Restricts the ability of the male to help Male mammals seek mating opportunities elsewhere


Biparental care

The most common form of care in birds Birds develop outside the mother’s body Male birds are as capable as their mates at providing

care Incubation, feeding, and guarding are divided equally Two parents are better than one


Male care in fishes and amphibians

Can be male-only care or with female care (biparental care)

In fishes and amphibians: usually a form of solitary male care

These animals rarely feed their offspring Parental duties consist of guarding Performed as well by one parent as by two


Biparental care in fishes and amphibians

Biparental care in fish: for survival and growth of offspring Evolved in ciclids ( 棘鰭類熱帶淡

水魚 ) because their broods face intense predation pressure

• Biparental care in discus: the brood attach themselves to both parents and feed off parental skin


Mode of fertilization affects patterns of parental care Reflect basic biological differences: where the young

develop and how they are fed Reflect ecological conditions (i.e. intensity of

predation) Teleost fishes, frogs and toads display four categories

of parental care in vertebrates: No care Male-only care Female-only care Biparental care


Patterns of parental care exhibited by some groups of vertebrates.


Diagram showing the major independent evolutionary transitions among modes of parental care in ray-finned fishes ( 輻鰭魚綱 ) .

Size of arrows reflects the relative numbers of evolutionary transitions, and numbers next to arrows indicate the range of evolutionary transitions estimated.


Fertilization and parental care

The association between mode of fertilization and mode of parental care relates to the proximity of adults and offspring

External fertilization in a territory defended by a male Is associated with male parental care

With internal fertilization The female carries the embryos And is in the best position to care for the young


Sex rolesGreater female investment in parental care

In many animals, females provide more parental investment than males Thought to explain sex differences in mating competition

The sex with greater parental investment (females) becomes a limiting resource, and An object of competition among individuals of the sex

investing less (males) Because of greater female investment, females select

mates Males compete for access to females This favors large body size and aggressiveness


Sex role reversal

The burden of parental care falls on the male When parental investment by males is greater

Males are choosy Females are competitive

Sex role reversal occurs in insects, birds, crustaceans, fishes, amphibians Overall, sex role reversed species are in the minority


Sex role reversal in northern jacanas

A polyandrous mating system: a female pairs with several males

Females defend a territory overlapping several male territories She plays a dominant role in courtship Females are much larger than males

Females back up males in confronting potential predators She’s more effective than the male at predator deterrence


African jacana

Males: build nests, incubate eggs, and care for and defend chicks.


Brood parasitism

Intraspecific brood parasites: lay eggs in conspecific’s nests Cliff swallows, red-fronted coots ( 大鷭 ) , wood ducks She may or may not lay eggs in her own nest

Interspecific (obligate) brood parasites: lay their eggs in other species’ nests They have no other reproductive option They never build nests Honeyguides( 響蜜鴷 ), Old World cuckoos( 杜鵑 ), New

World cuckoos, viduine finches, cowbirds, black-headed ducks

Ayo 教材 (動物行為學 2010) 40 black-headed ducks

Cliff Swallow red-fronted coots

wood ducks


Cowbird

Cuckoo Finch

黃嘴美洲杜鵑

Honeyguides ( 響蜜鴷 )


Raising young brood parasites

Host parents experience reduced reproductive success Damage is directly inflicted by a parasitic adult or its

offspring A female cuckoo may eat or throw out the host’s egg Or kill the young of the host Nestling cuckoos ( 杜鵑 ) evict ( 逐出 ) eggs or young

from the nest of their foster parents Nestling honeyguides( 響蜜鴷 ) kill young with whom

they share the nest


Brood parasites monopolize parental care

They mature more rapidly than a host’s young Their huge mouths and persistent begging elicit

preferential feeding The host’s young may die from starvation, crowding, or

trampling Parasitic young may benefit by keeping a few of the

host’s young around Host parents increase the rate at which they feed larger

broods Host parents may desert single chick broods


Host species try to avoid being parasitized

Host species conceal and defend their nests Identify and remove the eggs (or young) of parasites

Brood parasites try to deceive hosts Cuckoos lay eggs in the late afternoon when hosts are less

attentive Parasitic eggs or young resemble those of the host species

Common cuckoo egg

Great reed warbler egg


Whydah ( 寡婦鳥 )

Waxbills ( 織布鳥 )

Parasitic whydah( 寡婦鳥 )

Waxbill


Mating Systems

The ultimate goal of reproduction for both sexes is to maximize fitness (the relative number of offspring that survive and reproduce) The reproductive success of males and females is

constrained by different factors A male’s success is limited by access to females

While a female’s is limited by access to resources


Increasing reproductive success

A male can boost his reproductive success by mating with several females

A female increases her reproductive success by gathering more resources Including male parental care and access to a high-quality

territory Males focus on mating effort

Females emphasize parental effort Each parent tries to maximize its own reproductive

success Even if this is costly to the other


Classifying mating systems

Mating systems are defined based on the number of copulatory partners per individual per breeding season

Monogamy: a male and female have only a single mating partner per breeding season

Polygyny: males copulate with more than one female Polyandry: females mate with more than one male Polygynandry (promiscuity): both males and

females mate with multiple individuals


Ecological factors influence mating systems

Predation, resource quality and distribution, and availability of receptive mates affect the need for Parental care The ability of males to monopolize females The ability of females to choose among potential suitors

Ecological conditions vary Flexibility is associated with a species’ mating patterns

Black howler monkeys polygynous in a deciduous habitat polygynandrous in a riparian (riverside) habitat Monopolizing females by a single male is less likely in

the lush riparian habitat


Black howler monkeys


Sexual fidelity( 性忠貞 ) is hard to find in any system

Social monogamy exclusive living arrangement with one male and one female No assumptions about mating exclusivity or biparental care

Genetic monogamy: an exclusive mating relationship between one male and one female Very few species are genetically monogamous

Some socially monogamous fishes and mammals engage in extrapair fertilizations Cuckoldry is a problem for polygynous males

Extra-pair matings are the rule rather than the exception


Male extra-pair matings

A male’s costs: the time and energy in searching for receptive females other than his mate While he’s away, his primary mate may copulate with

another male Reducing his reproductive success

A male’s benefits: if he successfully inseminates mates of other males He can boost his reproductive success


Female extra-pair matings

Material benefits: A female gets help raising her offspring Extra-pair males defend the nest from predators Females exchange copulations for a valuable resource, i.e.

food Sufficient sperm may be provided to fertilize all her eggs

Genetic benefits: to obtain “good genes” for their offspring Post-fledgling survivorship of the young is related to the

genetic father Females of cooperatively breeding bird species avoid mating

with close relatives


Extra-pair matings in grey-crowned babblers

They live in social groups of a dominant breeding pair and nonbreeding helpers Members of the dominant pair may be related Extrapair young are found in the nest


Monogamy

Monogamy: male and female have only a single mating partner per breeding season

Sperm from one male is sufficient to fertilize a female’s eggs Monogamy is sufficient from the female perspective For males, confining copulation to a single female ensures

genetic representation in the next generation What ecological circumstances favor monogamy over

polygyny? Necessary biparental care Distribution of females Mate guarding


Monogamy and biparental care

When it is necessary or important for offspring survival Monogamy may be favored

Biparental care is more common among birds It’s rare in mammals

Males of some species have parental responsibilities And the fitness of both mates depends on the male’s

parental investment


Male California mice care for their young Fathers participate in all parental activities to the same

extent as mothers Once paired, these mice never stray( 走散 ) Pups are born at the coldest time of the year and need

their parents’ body heat to survive Both parents take turns huddling over the pups Removal of fathers resulted in lower pup survival


Male parental care in rodents

• The mound-building mouse is a monogamous rodent– Extended pregnancies of females without mates reflect

the high energetic costs of pregnancy and lactation


Monogamy and distribution of females

Distribution of females throughout the habitat influences mating systems

If it is hard for a male to monopolize multiple mates Circumstances will favor monogamy over polygyny

When receptive females are uniformly distributed i.e. because they defend exclusive territories Monogamy may evolve

If females are widely dispersed It is beneficial for a male to remain with a given female The male is at least assured of access to one mate


Symbiotic shrimp are monogamous

They live inside the mantle cavity of the pearl oyster Pearl oysters are small and scarce

Shrimp pairs consisted of a male and a female

Genetic monogamy may occur in shrimp Shrimp live in predator-rich

waters and are vulnerable when away from their hosts

Shrimp that leave may not be able to re-enter their original oyster


Monogamy and mate guarding

Monogamy may evolve if a male can guard only one female

Kirk’s dik-dik ( 柯氏犬羚 ) form permanent monogamous bonds Dik-diks seem to be faithful to their mates Genetic analyses revealed no evidence of extra-pair

paternity Why has such devotion has evolved in dik-diks?

Paternal care is absent—the male does not defend resources, reduce predation risk, or commit infanticide

Some monogamous males defend territories that could support more than one female

Females have ample opportunity to wander away


柯氏犬羚（學名 Madoqua kirkii ）

Kirk’s dik-dik ( 柯氏犬羚 ) ，分布於索馬里南部，肯亞中南部，坦尚尼亞中北部，安哥拉西南部和納米比亞。


Monogamy in dik-diks

Males prevent other males from knowing when she is in estrus He covers up the scent of his female’s dung by scratching dirt

and then defecating on top of it He marks his territorial borders with from glands under his

eyes If a male tried to overmark the scent of two females

He might fail to mark his territory sufficiently And lose ownership of the territory

The female accepts being guarded An extra-pair mating might cause a fight between her male and

the rival that could harm her or her offspring


Polygyny: costs and benefits for males

Polygyny: one male mates with more than one female during a breeding season

A male benefits by producing more offspring If paternal care is not required Males maximize reproductive output through multiple

matings Costs to a male:

An increased chance of cuckoldry since he does not guard each female

Costs associated with achieving dominance or defending resources or territories


Polygyny: costs for females

Males do not help rear the young If males do provide some parental care, it is divided

among offspring Or sometimes care is provided only to the first female

They must also share essential resources (nest sites or territories) Activity around these areas may attract predators

Other females may increase competition for resources


Benefits for females: the polygyny threshold hypothesis Polygyny threshold hypothesis: females gain advantages when

the benefits achieved by mating with a high-quality male And gaining access to his resources Compensate for the costs

A female may reproduce more successfully as a secondary mate on a high-quality territory Than as a monogamous mate on a low-quality territory

Polygyny threshold: the difference in a territory’s quality that make secondary status a better reproductive option for females Females join a harem when they have greater reproductive

success than monogamous alternatives


The polygyny threshold

The reproductive success of females decrease as the harem’s size increases

Female red-winged blackbirds prefer unmated males to already mated males But this is reversed if the territories of mated males are

superior to those of unmated males


Benefits for females: the sexy son hypothesis

Access to good genes for her offspring compensates a female for the costs of polygyny

A female may benefit if her sons inherit the genes that made that male attractive Her sexy sons provide her with many grandchildren

A female that chooses an already-mated male benefits indirectly If the good genes she acquires for her offspring boost

their survival and reproductive success


Types of polygyny: female defense polygyny

Female defense polygyny: a male defends a harem of females Females live in groups that a male can easily defend

Female gregariousness( 群居 ) is related to Cooperative hunting Increased predator detection Reproduction

Female elephant seals form dense aggregations Female gregariousness Shortage of suitable birth sites They return annually to traditional locations


Female defense polygyny in elephant seals

A single dominant male can monopolize access to 40 or more females This male defends his

harem Against all other male

intruders in bloody, and sometimes lethal, fighting


Types of polygyny: resource defense polygyny

Males defend resources essential to female reproduction (e.g., nest sites or food) Rather than defending females A male can monopolize a number of mates by

controlling critical resources Typical conditions include:

Quality of the monopolized resource reflects male quality

Females prefer males with resources over those without Males with resources have higher mating and

reproductive success


Females choose quality resources

A female’s choice is based on the quality of resources controlled by a male

Scorpionfly males fiercely defend the area around a dead arthropod The female must copulate to gain access to this food Larger males obtain larger arthropods Small males, unable to obtain arthropods, steal

copulations or present salivary secretions (a nuptial gift)


Scorpionfly ( 蠍蛉 ) Panorpa communis


Types of polygyny: lek polygyny

Males defend “symbolic” territories Located at traditional display sites called leks

Males do not provide parental care They defend only their small territory on the lek Not groups of females or resources


Two black grouse ( 黑琴雞 ) males displaying on a lek.


Females visit a lek to select a mate

Occurs when environmental factors make it difficult for males to monopolize females directly (female defense polygyny) Or indirectly (resource defense polygyny)

Male sandflies gather on the back of a vertebrate host and defend small territories Females visit these nocturnal leks and evaluate several

males But copulate with just one Some males copulate with many females Others will be unsuccessful at finding a mate


Sandfly


Evolution of lek behavior: the male’s perspective

Males may require specific display habitats That are limited and patchily distributed

Leks may provide protection from predators Through increased vigilance

Leks are information centers Males exchange news on good foraging sites


Hot spot vs. hot shot

Males gather near “hot spots” where females are most likely to be encountered

Less successful males have better mating chances near highly successful males (“hotshots”) Less successful males near hotshots obtain more

copulations


Evolution of lek behavior: the female’s perspective

Large groups of males may make mate choice easier To distinguish between superior and inferior males

It may reduce the vulnerability of females to predation A predator might be distracted by so many displaying

individuals Lek mating may reduce competition between the sexes

for resources


Polyandry

Polyandry: a female has more than one mate during the breeding season

Female reproductive success can increase with more mates If copulation includes critical resources or male parental

assistance Polyandrous insects increase the number of eggs laid

(clutch effect) and their hatching success Reduced risk of fertilization by genetically incompatible

sperm


Clutch effects and hatching success

Clutch effects are due to: Increased nutrients passed to females Increased receipt by females of hormonal stimulants in

male ejaculates Hatching success effects include:

Avoidance of sperm depletion Increased genetic diversity among progeny Reduced risk of fertilization by genetically incompatible

sperm


Honey bees are polyandrous

The queen mates with multiple males Increases genetic diversity

Drones: reproductive males Workers: infertile females

Closely related to the queen Diverse colonies:

More efficient at building combs Weigh more Survive winter Forage at higher rates Produce more workers and drones


Summary

Evolutionary decisions must be made about The amount of care and who assumes parental duties

Evolutionary conflicts over parental investment include Sexual conflict, intrabrood conflict, interbrood conflict

Avian brood parasites give up parental responsibilities Conflicts of interest characterize social behavior

Males produce more offspring by seeking additional mates Females emphasize parental effort and produce more offspring

by gaining male parental investment Mating systems are affected by ecological factors (predation,

resource quality and distribution) and availability of mates


Summary

Monogamy: a male and female have a single partner per breeding season

Polygyny: males copulate with more than one female Polyandry: females mate with multiple males during the

breeding season Polygynandry: both males and females mate multiple

times Extra-pair matings are common

Benefits to males: increased number of offspring Females gain help in raising offspring, obtaining food,

genetic benefits, fertility insurance, high-quality genes


問題與討論

[email protected]

Ayo 台南 NUTN 站 http://myweb.nutn.edu.tw/~hycheng/

親代照顧和交配體系 (parental care and mating systems) ─ 動物行為學 (ethology)...

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