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

1. The Evolution of Parental CareChapter 12 Alcock (Animal Behavior)Tom Wenseleers Ethology & Behavioural Ecology

2. Plan of lecture • Costs and benefits of parental care • Parent-offspring conflict • Maternal, paternal & biparental care • Parental favoritism & siblicide

3. 1. Costs and benefitsof parental care

4. 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.

5. 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.

6. 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.

7. 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.

8. 2. Parent-offspring conflict

9. 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 parentshares 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.

10. 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.

11. 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.

12. 1Hirunda rustica 2Tachycineta bicolor 3 Sialia sialis 4 Prunella modularis 5 Passerina cyanea 6 Melospiza melodia 7 Zonotrichia leucophrys 8 Calcarius lapponicus 9 C. pictus 10 Agelaius phoeniceus 11 Molothrus ater a b c d e 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 -10 -20 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)

13. 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.

14. Siblicide Spadefoot toads Sand tiger sharks Piglets Masked booby Kittiwake gulls Indian rosewood

15. 3. Maternal, paternal& biparental care

16. 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.

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

18. 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.

19. 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.

20. 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)

21. 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.

22. 3. Intra- and interspecificbrood parasitism

23. 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.

24. 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%).

25. 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

26. 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?

27. 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.

28. 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.

29. 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

30. 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.

31. 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.

32. 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

33. 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.

34. 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.

35. 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.

36. 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.

37. 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.

38. RenestingNo renesting 12.18

39. 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.

40. 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.

41. 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.

42. 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.

43. 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.

44. 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.

45. 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.

47. 4. Parental favoritismand siblicide

48. 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.

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

50. 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.