Lecture Notes VI - Parental Behavior

Parental decisions:

1 - Males or females?

2 - Quality or quantity?

3 - How much should be invested in reproduction?

4 - How much should be invested in caring for young?

Males or females?

In most species, the sex ratio is about 1:1. Why? Does meiosis guarantee equal numbers of males & females? No, sex ratios in some species are known to depart from unity in ways that appear to be adaptive (Fisher 1958).

Imagine a population with many more females than males. If parents could select the sex of an offspring, what would it be? Male, because with an excess of females, the 'average' male will produce more offspring than the average female. Thus, selection pressure favors production of the 'rare' sex.

FISHER'S ARGUMENT applies only if parents have no information concerning the future competitive abilities of their offspring. But, what if parents have such information?

• Trivers & Willard (1973):
• There may be circumstances in which parents might profit by producing one sex or the other.
• In general, produce males when dominant and/or in good physical condition and produce females when subordinate and/or in relatively poor condition. ---> WHY?
• Males exhibit greater variance in reproductive success, so a good quality or dominant male may have increased reproductive success.
• Poor quality males will have lower reproductive success, so parents may maximize fitness by producing females.

• McClure (1981):
• Well-fed female wood rats (Neotoma floridana) ---> invest equal amounts of energy in sons & daughters which wean at about the same weight; males grow further after weaning
• Food-deprived females:
• channeled 68% of transferred energy to daughters & only 32% to sons
• Many males died & those that survived grew more slowly & were weaned at lower weights than females
• Discrimination against males was direct; food-deprived females removed sons from nipples to permit daughters to suckle

• Barash (1982):
• Humans may bias investment toward either males or females, depending on which will maximize parents' fitness.
• Check 'Relationship of socioeconomic status to reproductive opportunities and mobility among human beings'

Sexual conflict can interfere with biparental care reducing the quality of offspring (Royle et al. 2002).  The cost of investment in some biparental regimes (both parents rearing the young) can cause a sexual conflict by one parent reducing the amount of care given to the offspring in order to preserve energy for another partner. This theory was tested with zebra finches (Taeniopygia guttata).  Biparental regimes (male and female) were formed to rear four young and uniparental regimes (female alone) were formed to rear two young.  After fledging of the brood, the females from the uniparental regimes were re-introduced to male partners to form biparental regimes and the females from biparental regimes became single mothers to lay another clutch of eggs. Male chicks from both parental regimes were tested as adults for sexual attractiveness to experienced females.  By keeping the potential workload to rear the young constant in both regimes, the young from the uniparental regimes received 25% more parental investment than their siblings in the biparental regimes. In biparental regimes, it was found that males gave equal or more parental investment than their female partners, suggesting that females preserved energy for another partner. This would be in accordance with the finding that the mass of the second clutch of eggs laid was lower for the post-uniparental females than the females from the post-biparental regimes. It seems that more effort for quality in rearing young is giving by a single-parent, whereas both parents give more effort for quantity. The effect of quality could also explain why males reared in uniparental regimes were sexually more attractive as adults than their male siblings reared in biparental regimes. These findings suggest that sexual conflict in pre-zygotic (mating) and post-zygotic (parental investment) may be a force that shapes the sexual selection.                                                                                                                             -- contributed by Stephanie McIntosh

Potential problem: More offspring mean less investment/offspring & increased investment/offspring means fewer offspring. Which strategy is best?

• r-selection vs. K-selection = extremes on a continuum:
• r-selection ---> maximize r (= rate of population increase)
• K-selection ---> maximize survival & reproduction when population size is at or near K (= carrying capacity)

• r- vs. K-selection is relative. A species is only K-selected in comparison with a more r-selected species, e.g.:
• Most invertebrates are r-selected compared to vertebrates
• Tree squirrels are K-selected compared to ground squirrels but rodents are r-selected compared to elephants, etc.

How much should be invested in reproduction?

Reproductive effort:

• proportion of total energy devoted to reproduction during a given time interval
• should maximize reproductive value

How much should be invested in caring for young?

• Distribution of parental care among species:
• Why do some species show elaborate & protracted care while others do not?
• Why are males responsible for care in some species, females in others, & both sexes in a few?

• Parental care might be expected when young face:
• Physically harsh environments
• Heavy predation
• Intense competition with conspecifics

• Who cares for young?? What's the influence of gamete size?
• Trivers (1972):
• Females should usually be the care-giving sex because the costs of producing ova exceed those of sperm, committing deserted females to continue investing to avoid wasting their reproductive effort = CONCORDE FALLACY
• Dawkins & Carlisle (1976):
• Each sex should decide whether or not to prolong investment on the basis of likely net benefits in the future.

• Four evolutionary stable strategies (Maynard Smith 1977):

1) Both sexes desert - requires that neither male nor female does better (in terms of surviving young) by providing care

2) Female deserts & male cares ('stickleback strategy')

• No difference in survival of young relative to presence or absence of female care
• Egg survival with uniparental care must exceed survival of uncared for eggs multiplied by the number of matings that a non-caring male can achieve, or male will desert


3) Female cares & male deserts ('duck strategy')

• Possible if a male who deserts has a good chance of mating again


4) Both partners care

• Reproductive success must be greater than if male or female deserts

How much should be invested while caring for young? -- Parental allocation of resources should evolve as a balance between the needs of current and future reproductive success.  One assumption in the prediction of this balance is that organisms may use different foraging options in self-feeding, and feeding of offspring.   Palestine sunbirds (Nectarinia osea) exhibit food-type separation between parent (nectar) and offspring (arthropods).   Manipulation of parent nectar concentrations was shown to have a significant influence on parental investment and roles (Markman et al. 2002).  As sugar concentrations increased, nest visitation by both sexes increased.  Female delivery rate of arthropods (and thus increased energy intake of the offspring) and time spent at the nest increased, while male sunbirds increased the amount of time mobbing.  This experiment indicates that parents may invest more in their young when their own energy intake increases, and may invest more in certain sex-dependant roles when energy intake allows for this separation (Markman et al. 2002).                                                          - Contributed by Aimee Wilson

Photo: www.birdingisrael.com/birdingHeb/content/reportsHeb/ inFocus/palestine-sunbird.htm

• Response of partners to changes in level of investment by mates:

• Mate removal experiments - remaining parent typically compensates (partly or fully) for the reduction in assistance by their 'missing' mate (e.g., Northern Mockingbirds, Savannah Sparrows, & others)
• 'Weighting experiment' with European Starlings (Sturnus vulgaris)
• weights attached to tails = reduced feeding rates
• RESULTS = unweighted mates compensate, but not fully

• Given such compensation, why is biparental care so common among birds?
• BEST EVIDENCE = Male removal experiments ---> in many altricial birds, removal of males reduced growth rate of young, survival of young, or survival of fledglings before independences, e.g., in Dark-eyed Juncos, the removal of males within 2 days of hatching had little effect on nestling survival but did influence survival of fledglings

Parental care and reproduction in Mantidactylus (Lehtinen 2003)  -- Parental care in anurans is relatively uncommon, exhibited in only 10-20% of extant species. The most common type of parental care is egg attendance, with a parent remaining with an egg mass at a fixed location. Typically, egg attendance is performed by either the male or female, depending on the species. Less common is amphisexual egg attendance, where either the male or female attends the eggs but not both. Amphisexual egg attendance has been observed in two species of rain forest frogs from Madagascar, Mantidactylus punctatus and M. bicalcaratus. Over a period of two years, observations revealed that egg attendance was performed almost exclusively by females in M. bicalcaratus but in M. punctatus egg attendance was performed by males or females with equal frequency. Decreased predation of eggs, hydration, prevention of fungal infection and reduced chance of developmental abnormalities are benefits of egg attendance. Costs include loss of breeding opportunities, increased vulnerability to predators and decreased feeding opportunities. Males may only attend to egg masses when the availability of mates is low or amphisexual egg attendance may only be a transitional trait that will eventually evolve into either maternal or paternal care.                                                                  - Contributed by Jodi Stacy

Mantidactylus bicalcaratus © 1994 Frank Glaw

Parent-offspring conflict (Trivers 1974):

• result of natural selection operating in opposite directions on the two generations. Parents & offspring share only ½ of their genes. As a result, there comes a time when it is more profitable for a parent to 'dump' offspring & devote efforts to production of another offspring. At this time, 'conflict' may occur.

• When should this conflict occur?
• perhaps most intense as young approach independence but can occur anytime, i.e., when interests of both mother & offspring are served when parent helps BUT disagreement exists over how much help is to be given.
• such conflict results because the parent seeks to invest such that difference between costs & benefits is maximized while offspring seeks to maximize difference between benefits & ½ cost (cost is devalued by coefficient of relatedness which is 1/2).

• Examples of P-O conflict?
• http://www-personal.umich.edu/~phyl/anthro/conflict.html
• http://academic.dt.uh.edu/~williams/child/conflict.htm

• Strategies of parents & offspring are not fixed; they may be able to negogiate (e.g., tit-for-tat) (Godfray 1991):

• Offspring should provide 'honest' information about needs
• Honest information should be most important whenever offspring condition is highly variable (parents need more information then), e.g., transition to independence. Intensified signaling (what appears to be increased demands) can be mutually beneficial at this time (& not necessarily 'weaning conflict').

Begging

• Means for nestlings to communicate nutritional needs to parents?
• Can be costly for 2 reasons:
• might attract predators
• might be energetically costly
• If begging functioned only for communication, wouldn't it be less conspicuous?

Assume investment by parents is some fixed value, then each nestling may try to manipulate parents and outcompete siblings to get a larger share of this investment. Do nestlings do this??

• Experimental evidence (Smith & Montgomerie 1991):
• American Robins (Turdus migratorius):
• Nestlings that begged most vigorously were most likely to be fed
• Nestlings that were hungrier begged more vigorously
• Nestlings responded to increased begging intensity of a sibling by begging more vigorously themselves

Should siblings put some limit on begging intensity? Perhaps they should because:

• allowing siblings to feed may enhance their inclusive fitness, and
• intense begging could attract predators which would, of course, reduce a nestling's fitness.

• Loudness of begging calls increases as the relatedness among members of a brood declines. Species with high levels of mixed parentage, as well as young Brown-headed Cowbirds, beg louder than their closest monogamous and non-parasitic relatives. SO, nestling birds have responded over evolutionary time to a reduction in average relatedness among nestmates by behaving more selfishly and begging louder. An upper limit to begging intensity will be set by the loss of fitness, both directly & through kin.

Literature cited:

Barash, D.P. 1982. Sociobiology and behavior, 2nd ed. Elsevier, NewYork.

Dawkins, R. & T.R. Carlisle. 1976. Parental investment, mate desertion and a fallacy. Nature 262:131-133.

Fisher, R.A. 1958. The genetical theory of natural selection, 2nd ed. Dover Press, New York.

Godfray, H.C.J. 1991. Signalling of need by offspring to their parents. Nature 352:328-330.

Godfray, H.C.J. and R.A. Johnstone. 2000. Begging and bleating: the evolution of parent-offspring signalling. Trans. Roy. Soc. Lond. B 355:1581-1591.

Huber, S., E. Millesi, and J.P. Dittami. 2002. Paternal effort and its relation to mating success in the European ground squirrel. Animal Behaviour 63:157-164.

Lehtinen, R.M. 2003. Parental care and reproduction in two species of Mantidactylus. Journal of Herpetology 37: 766-768.

Markman, S., B. Pinshow, and J. Wright. 2002. The manipulation of food resources reveals sex-specific trade-offs between parental self-feeding and offspring care. Proceedings of the Royal Society Biological Sciences Series B 269: 1931-1938.

Maynard Smith, J. 1977. Parental investment - a prospective analysis. Anim. Behav. 25:1-9.

McClure, P.A. 1981. Sex-biased litter reduction in food-restricted wood rats (Neotoma floridana). Science 211:1058-1060.

Royle, N.J., I.R. Hartley, & G.A. Parker. 2002. Sexual conflict reduces offspring fitness in zebra finches. Nature 416:733-736.

Smith, H.G., and R. Montgomerie. 1991. Nestling American Robins compete with siblings by begging. Behav. Ecol. Sociobiol. 29:307-312.

Trivers, R.L. 1972. Parental investment and sexual selection. In: B. Campbell (ed.), Sexual selection and the Descent of Man. Aldine, Chicago.

Trivers, R.L. 1974. Parent-offspring conflict. American Zoologist 14: 249-264.

Trivers, R.L. & D.E. Willard. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90-92.

Useful links:

Driving parents cuckoo

Kin recognition; parent-offspring interactions

Need & nestmates affect begging in Tree Swallows

Sex-biased hatching order in House Finches

Signals of need in parent-offspring communication and their exploitation by the common cuckoo

Why are there males and why so many?

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