1. The Evolution of Communication Chapter 9 Alcock (Animal Behavior) p. 282-313 p. 275-281: not for exam Ethology & Behavioural Ecology Tom Wenseleers

2. Communication Definition: the transfer of information from signaler to receiver Two evolutionary puzzles: – How can signals evolve? – What mechanisms can maintain signal honesty and prevent deception?

3. 1. The evolutionary origin of signals

4. Problem For an effective signal to evolve an animal not only needs to acquire the ability to produce the signal but others also needs to be able to detect and respond to such signals How can this ever evolve?

5. Male whistling moths Male whistling moths use ultrasound pro- duced by modified forewings ("castanets") to communicate. Some related ancestors are preyed upon by bats, and in response these moths evolved the perceptory machinery to hear bat-produced ultrasound waves. So perceptual machinery was in place and this may have led to the evolution of a special organ to produce ultrasound for communicative purposes. (they themselves do not have bat predators)

6. Co-option of an ancestral signal In most or all bowerbirds (tuiniervogels) males use the "skraa" call to threaten rivals. In one cluster of closely related species, this signal now also serves a courtship role.

7. Sensory exploitation & biases Sensory exploitation: when signal givers tap into preexisting perceptual mechanism; leads to sensory biases. Example: courtship by male water mites. (A) Female is in prey-catching position. The male approaches and waves a trembling foreleg in fron of her, setting up water vribations similar to those a copepod might make. Female may respond by grabbing him, but releases him unharmed. (B) The male then deposits spermatophores in front of the female.

8. Preexisting sensory biases Male and female guppies eat Clusia fruits which are orange due to the presence of carotenoids. The same carotenoids also accumulate in males and lead to colourful patterns. Observation: females prefer colourful males. Why? Preexisting sensory bias for detecting orange fruits.

9. Preexisting sensory biases Mate preferences for a novel male ornament: females prefer white crested males. Why? Perhaps because they line their nest with white feathers.

10. 2. The maintenance of signal honesty

11. What mechanisms favour honest communication? J. Maynard Smith & B. Harper (2003) Animal Signals. Oxf Univ Press. 3 ways that signals may be honest/reliable: 1. Common interest dance language in honeybees: incl. fitness benefits communication within a body raven yelling: mutualistic benefits plant-insect communication: mutualistic benefits 2. Handicap/cost begging by bird chicks male displays used to attract females 3. Index of quality (uncheatable signals) loudness and depth of calls by males body size

12. Signal honesty due to common interest ExampleSignaller What is the benefit of producing the signal? Receiver What is the benefit of acting on the signal? Communication within your body Your head Increase survival of organism and help the transmission of copies of the gene(s) responsible for the signal Your leg Increase survival of organism and help the transmission of copies of the gene(s) responsible for signal reception Honeybee dance language Dancing bee Increase colony productivity and the bee’s inclusive fitness. Dance following bee Increase colony productivity and the bee’s inclusive fitness. Raven communication Yelling raven Increase chances of establishing a territory. Other ravens Being guided to food. Plant-insect communication Plant Signal nectar availability and get pollinated. Insect Obtain more food (nectar).

13. Honest communication due to common interest Example: insect societies

14. Dancer (forager) "Signaller" Dance followers (unemployed foragers) "Receiver" Karl von Frisch: 1973: Nobel Prize Angle of waggle run correlates with angle of food source relative to the sun; duration of waggle run correlates with distance of food source; total number of waggle runs correlates with the quality of the food source Waggle dance

15. Tremble dance performed by returning foragers with nectar who experience long unloading delays to receiver bees consists of irregular movements in all directions recruits more nectar receiver bees and also reduces the amount of foraging

16. Alarm pheromone Produced by Koschevnikov gland, near sting shaft Consists of more than 40 chemical compounds, including isopentyl acetate (IPA)

17. Communication in leaf-cutting ants Leaf-cutting ants stridulate to recruit other cutters and minims, which protect the leaf-carrying ants against parasitoids and help maintain pheromone trails pheromone trail fungus garden hitchhiking minims

18. Queen egg marking In honeybees workers can lay eggs but such eggs are eaten by other workers ("worker policing") Workers benefit from policing because they are more related to the sons of the queen (r=0.25) than to the sons of other workers, many of which are half-nephews (r=0.125) (honeybee queens mate with ca. 10 males) Ratnieks & Visscher Nature 1989

20. Queen egg marking Workers can tell worker-laid from queen-laid eggs because the queen marks her eggs with a pheromone The queen (signaller) benefits from producing the signal because it protects her eggs The workers (receivers) benefit from it because they will end up rearing the more closely related male offspring of the queen

21. Dishonest communication due to divergent interests in insect societies

22. Anarchistic bees Rare lineages of anarchistic bees: workers lay eggs that mimim the smell of queen-laid eggs Such eggs are not policed Usually displayed by workers from one particular patriline Benefits the rare workers that produce such deceptive signals because they end up producing sons (r=0.5) or full-sisters' sons (r=0.375) rather than brothers (r=0.25) Oldroyd et al. Nature 1994

24. Communication honesty in insect societies Common interests are strong –Individuals are related to each other –Food collected by different workers feeds the same, related brood –Usually leads to honest/reliable communication But conflicts can occur –Can lead to deception in communication –Particularly over reproduction –Relatedness of 1 would eliminate all potential for conflict (e.g. cell-cell relatedness in multicellular organism)

25. Honest communication due to common interest among nonrelatives: raven yelling

26. Benefits of raven yelling Background Large mammal carcasses are rare. But can be valuable resource to Maine ravens in winter. Once carcass could provide months of food. Observation Many ravens were seen feeding on a dead moose. Puzzle Ravens are rare Would need to call ravens from other groups Would not be relatives Question What is the benefit of communicating (yelling)?

27. Hypotheses for adaptive significance Attract a "carcass opener" such as a bear (and incidentally more ravens) AgainstLone ravens finding a carcass did not yell AgainstRavens at an opened carcass sometimes did yell Selfish herding: attract more ravens in case of attack AgainstYelling continued at carcasses with many ravens Overwhelm defence of territory holding ravens ForTerritory holding ravens did not yell ForNon resident ravens did yell ForYelling attracted other ravens to a carcass ForTerritory holders unable to repel many non residents ForCarcasses eaten by 1 or 2, or by many ravens

28. Raven yelling Communication or non-communication are both favoured by common interests. Territory holders are better off if they don't yell, in order to monopolise a carcass. Non-residents are better off if they yell, in order to attract others to defend the carcass against residents.

29. Honest communication due to common interest in interspecific interactions Example: plant-insect communication

30. Nectar guides nectar guides: guides insects to nectar plant gets pollinated at same time horse chestnut: nectar guide is yellow when it produces nectar; when flower stops producing nectar it turns red both parties benefit: plant gets pollinated more effectively, insect can collect more nectar since it signals the timing, not the amount of nectar secreted, there is no incentive for the plant to provide deceptive signals

31. Honest communication due to costs: begging in chicks

32. Begging chicks & feeding parents Why do chicks beg? Background Parents often give more food to chicks that beg more. Begging can attract predators. How can begging be an honest signal of need? Evolutionary argument: cost-benefit. Testing cost-benefit predictions Effect of relatedness (extra-pair parentage) Exploitation of parents by begging Brood parasites

33. Why feed chicks who beg more?

34. Parents feed begging chicks more Pied flycatcher birds. Only one parent heard a taped begging call at the nest. The other heard no call. The parent who heard the call, whether male or female, responded by bringing back more food. Thus, on the left the female brings back more food when she hears begging (upper inverted triangle) than when she does not (lower triangle). Pied flycatcher (bonte vliegenvanger)

35. Costs of begging: nest predation Begging is also costly. There is the cost of making the calls, but more importantly it increases net predation. The cost to the chick is losing its own life, but also losing the lives of siblings (Hamilton's rule). In this study artificial nests were more likely to be predated if begging calls (from two species) were played. The black-throated blue warbler ("blauwe zwartkeelzanger") is a tree nester, and the ovenbird ("ovenvogel") a ground nester. The begging calls of tree nesters attract more predators. But predation risk in trees is lower than on the ground, so tree nesters beg more loudly.

36. Adaptation in warbler begging calls Chicks of ground-nesters which are more prone to predation produce higher-pitched begging calls, and high-frequency sounds do not travel as far.

37. How can begging be an honest signal? A. How can begging by chicks be an honest signal of need for food? B. Why don't chicks beg maximally whatever their need? If a chick that begs more gets more food (A) and if more food increases survival, why don't chicks then beg at the maximum intensity (B)? But if they do this, then there should be no correlation between begging intensity and need for food (B). As we will see, if there is a cost to begging this can lead to begging intensity being correlated with the need for for food (A).

38. The more the chick begs the greater the predation risk to the nest. The effect is probably linear or close to it. Thus, if the chick begs for 60 minutes not 30 minutes it will double the chance of attracting a predator. Costs to chick from begging more

39. Benefits to chick from begging more The more the chick begs the more food it is given by its parents. But the curve shows decreasing returns as each additional increment of food is worth less to it in terms of increased survival.

40. The optimum begging intensity for chick 1 is where the difference between cost and benefit are greatest. Benefits to chick from begging more

41. Now we consider a second chick who is less in need of food. For chick 2, the extra food obtained by any level of begging is worth less to it in terms of increased survival than for the hungry chick. So chick 2's optimum level of begging is less. As a result, there is a correlation between hunger level and begging intensity.

42. Benefits to chick from begging more In this example, we can see that lowered predation risk, such as from tree nesting, results in higher optimum levels of begging. But the optimum level of the hungry chick is still more than for the less hungry chick.

43. Begging & relatedness a b c d e 1 Hirunda rustica 2 Tachycineta 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 abcdeabcde Species pair Volume of begging calls (dB) -40-30 -20 -10 1 2 3 4 6 7 8 9 10 11 Black: high relatedness (monogamous) Red: low relatedness (frequent extrapair copulations or socially parasitic) Also inclusive fitness costs due to increased predation of siblings. Results in louder optimal begging calls in species with lower chick-chick relatedness. Lower relatedness results in louder calls brown headed cowbird

44. Honest communication due to costs: revealing handicaps in males

45. Signalling quality with a costly display This imaginary example considers the costs and benefits to a male of making a large display. The display is attracting to females (double mating success) but reduces survival. The survival cost is greater to low quality males. So only high quality males benefits (survival x matings) from making a display. The display is an honest signal of quality, a handicap that only high quality males can afford.

46. Amotz Zahavi

47. Human example of a Zahavian handicap conspicuous consumption Conspicuous consumption is a trait not easily faked, and is an honest indicator of those who possesses resources.

48. Honest communication due to uncheatable indices of quality: body size

49. Toad calls

50. Male toads with a female were gagged so that they could not call. Taped calls were then provided at either low or high frequency. Low frequency calls deterred rival males more than high frequency calls. In general, larger toads make deeper calls. Small toads cannot easily make deep calls. Therefore, deep calls are an honest signal of male size and likely ability to deter a rival.

51. Cheating body size possible up to a point inflating abdomen puffing out chest making hair stand on end elongating larynx to make deeper calls

52. Honest signals are expensive In the side-blotched lizard, males that have run on a threadmill to lower their endurance are not able to maintain their threat posture for as long, and generate fewer pushup displays.

53. Honest signal in antler flies Antler fly males confront each other head-to-head. The head projections are large, elaborate & expensive to produce. Antler span and eye span are closely correlated with body size.

54. Honest signals in red deer Only red deer stags in top condition can roar for long periods.

55. Deceptive communication between species

56. Brood parasites: cuckoo Cuckoos are brood parasites. One cuckoo chick displaces an entire brood of reed warbler chicks. The begging intensity of one cuckoo chick (D) is similar to an entire brood of reed warbler chicks (C) and much greater than a single reed warbler chick (B).

57. Brood parasites: cuckoo The begging of one cuckoo chick is as effective at causing the reed warbler parents to feed it as the begging of an entire brood of warbler chicks.

58. Brood parasites: cuckoo Why does the reed warbler listen to the cuckoo signal? Of course it would be selected to try to detect cuckoos and not feed those chicks But this may be costly since the erroneous underfeeding or rejection of an own chick would greatly reduce the warbler's fitness

59. Sexual deception Mimicking female to attract and eat male Fire fly femme fatale (Note: fire flies are beetles, not flies) Bolas spider Why is a male attracted? Males are still attracted because, on average, following the signal will increase his fitness because mimics are relatively rare. Even a single mating with a female will bring high fitness.

60. Deception: fire fly femme fatale Male Photinus fireflies are attracted to species-specific flashing of female. Another predatory firefly (Photuris) mimics this, and the amorous male is killed.

61. Deception: bolas spider The bolas spider attracts moths by mimicking the female moth's phero-mone. Only male moths of one or two species are caught. The moth is caught on a sticky line that the spider swings in a circle beneath it.Ignoring the female sex pheromone would impose a large cost.

62. Deception: anglerfish Anglerfish have a lure that looks like a small prey item to smaller fish. It then preys on these smaller fish. Again, the smaller fish will always be selected to respond to such visual stimuli because not doing so would lead to starvation.

63. Signal exploitation by other species

64. Origin of the honeybee dance language bumblebees: use scent to mark the location of food sources more derived honeybees and stingless bees: use dances or sounds to communicate the location of food sources hypothesis: strategy to avoid other species or other unrelated colonies from evesdropping on scent-marked food sources?

65. Illegitimate receivers Females of the tungara frog prefer males that give whining calls with chucks (blue in sonogram). However, males that emit such calls are more likely to be preyed upon by fringe-lipped bats.

66. Avoiding signal exploitation "Seet" call of the great tit: alarm call used when a flying sparrow hawk is seen Is a high frequency call that is not easily heard by sparrow hawks; also does not travel large distances. (sperwer) (koolmees)

67. Convergent evolution of "seet" call