Proximate and ultimate causes of bird song

1. Proximate and ultimate causes of bird song • Different species of bird (and other organisms) sing different songs. • How? What proximate mechanisms control how birds learn to sing and the mechanics of how they sing? • Why? What selective advantage does singing provide?

2. Gene and environment interactions • Singing mechanism (syrinx [or voicebox], nerves, muscles) has complex development process. Genes are heavily involved. • Type of song sung also affected by environment i.e., songs heard.

3. Differences between individuals in song can result from differences in genes or environment (or some combination).

4. Song dialects in White-crowned Sparrows

5. Song dialects in White-crowned Sparrows • Peter Marler and colleagues carried out extensive work on songs on White-crowned Sparrows in San Francisco Bay area. • Different areas have distinctly different songs

7. Song dialects in White-crowned Sparrows • Were differences due to genes or environment? • Birds were hatched and reared in isolation. Males began to sing at about 150 days of age, but did not sing full complex song of wild birds.

8. Song dialects in White-crowned Sparrows • Do young birds need to be hear songs to learn them? • Young birds were exposed to tapes of singing males between 10-50 days of age. • Began singing at about 150 days and by age 200 days closely mimicked song they had heard when younger.

9. Song dialects in White-crowned Sparrows • When developing song, sparrow must be able to hear itself sing apparently so it can compare its song to that it heard when younger. • Birds deafened after 50 days do not develop proper song.

10. Song dialects in White-crowned Sparrows • White-crowned Sparrows are also selective about which songs they will learn. • If exposed only to songs of another species when young WC sparrows ultimately do not develop a proper song. • If exposed to songs of many species as well as its own WC Sparrow produces a normal song.

11. Song dialects in White-crowned Sparrows • Marler concluded that immature WC Sparrow brain during critical period selectively stores information about songs of WC Sparrows and ignores other species. Later accesses this information to develop it own song.

12. Song dialects in White-crowned Sparrows • In wild WC Sparrows sometimes sing non-WC songs of other species. • Baptista and Petrinovich hypothesized that being exposed to living birds rather than tapes might cause this.

13. Song dialects in White-crowned Sparrows • Hand-reared WC Sparrows exposed to singing Song Sparrows and Strawberry Finches they could hear and see learned the other species song even if they could hear tapes of WC song. • Social experience thus can have a strong effect on WC Sparrow singing behavior.

15. Song dialects in White-crowned Sparrows • In summary, in proximate developmental terms W-C Sparrows are influenced when young by their social and auditory environment and construct a memory of the song they should sing. • Later they use this model to develop their own song.

16. A natural experiment in call learning: Galahs reared by Pink Cockatoos. Birds similar in appearance, but have different begging, contact, and alarm calls. Galah

17. Mixed clutches sometimes occur when birds share nest holes. Pink Cockatoos rear chicks. Pink Cockatoo

18. Adopted Galahs reared in Pink Cockatoo social environment. As adults join Pink Cockatoo flocks.

19. How are calls affected? • Galah chicks give normal Galah begging and alarm calls, but give Pink Cockatoo contact calls.

20. Sonagrams of Galah and Pink Cockatoo contact calls

21. Contact calls used constantly in flocks. • Galahs learn to give a call Pink Cockatoos will respond to. • Pink Cockatoo social environment overrides genetic differences between species underlying contact call.

22. Neural mechanisms of song • The brain obviously plays a major role in singing and song learning. • In most species only males sing so we would expect there to be differences in brain structure between males and females. • Differences could be genetic or environmental (or both).

23. Neural mechanisms of song • In Zebra Finches only males sing. • What mechanism explains this difference between the sexes?

24. Neural mechanisms of song • Pre-testicular cells in male embryo produce estrogen. • Estrogen travels to nerve cells in the brain and is transformed into a testosterone-like hormone. • Complex neural system (the song system) is then stimulated to develop

25. Clusters of cells called song control units form in the brain. Nerve connections formed between front of brain and syrinx (voice box).

26. Higher vocal complex Caudomedial neostriatum Robust nucleus of arcopallium Area X You don’t need to learn all these names! (carries signals to syrinx)

27. Neural mechanisms of song • Neural connections formed in male zebra finch’s brain in first 40 days after hatching. • In females, equivalent part of brain shrinks through cell death.

29. Neural mechanisms of song • Estrogen is the crucial signal molecule for brain development in zebra finches. • Females given estrogen within 4 days of hatching develop song system in brain. • But, females don’t sing later unless given testosterone implants as adults.

30. Neural mechanisms of song • Development of male’s brain and structures needed to produce full song follows highly coordinated pattern. • Genes turn on and off in various parts of the brain in a predictable coordinated fashion.

31. Enzyme activity in brain. Intensity of color correlates with gene activity

32. Neural mechanisms of song • Scientist’s ability to monitor gene expression in the brain is providing insight into what genes affect the brain’s structural changes. • For example, male Zebra Finches go through a period when they attempt to match what they are singing to stored memories of songs. • During the process, cells in forebrain become progressively more responsive to male’s own song rather than to tutor songs.

33. Neural mechanisms of song • As finch tries to match tutor’s song, the activity of a gene called ZENK increases in some song control neurons including area X in bird’s forebrain. • Listening to itself sing causes increase in gene activity that increases protein production, which presumably alters neural circuits in that area of the brain.

34. Neural mechanisms of song • As male’s song becomes a closer match to the tutors ZENK gene activity falls, presumably because when bird can sing the tutor’s song no further alterations to the brain are needed.

35. High activity of ZENK gene in area X (yellow area)

36. How avian song control system works • Song control systems in birds includes several clusters of neurons (called nuclei) • Nuclei are connected together by long extensions of neurons (axons). • Some components involved in song learning, others in song production.

37. How avian song control system works • The HVC or (higher vocal center) is a dense collection of neurons • HVC connects to the RA (robust nucleus of the acropallium) which then connects to the syrinx or (voice box) via nXIIts (tracheosyringeal portion of the hypoglossal nucleus).

38. Higher vocal complex Caudomedial neostriatum Robust nucleus of arcopallium Area X You don’t need to learn all these names! (carries signals to syrinx)

39. How avian song control system works • The connection of HVC and RA to the syrinx suggests these brain areas control singing. Cutting connections between RA and syrinx has severe effects on singing. • RA in male birds is also larger than in females consistent with a role in singing.

40. Difference in size of one nucleus of the song system in brain. Robust nucleus of the Arcopallium (RA) much larger in male than female. Male Zebra Finch (left) female (right

41. How avian song control system works • Other areas of brain such as LMAN appear to be more important in song learning. • In Zebra Finches destruction of this area in brain before bird has learnt to sing prevents it producing a proper song as an adult, but destruction after learning song has little effect on the song produced. • Consistent with the idea that LMAN is involved in song learning is that in birds that don’t learn their songs that the LMAN is missing or reduced in size

42. How avian song control system works • HVC also appears to be important in song learning. • In species in which males learn their songs, the larger the repertoire males of a species sing the larger the HVC is.

43. How avian song control system works • But does learning a lot of songs cause the HVC to grow or is it necessary to have a large HVC to learn them? • How could we distinguish between these two possibilities?

44. How avian song control system works • Raise two groups of birds under different conditions (in isolation or with males to learn from) and compare their brains. • Male sedge warblers reared in isolation have HVCs indistinguishable from those of males who learned songs from tutors. • Supports idea that HVC needed to learn.

45. Neural mechanisms of song: Conclusions • A bird’s song is product of a complex series of systems in the brain that regulate the learning and production of the song. • Brain develops as the result of gene-environment interactions in which environmental stimuli both internal (e.g. hormonal) and external (hearing songs) cause changes in gene activity in certain portions of the brain, which shape the brain’s development.

46. Ultimate explanations for birdsong • Song learning occurs in three of 21 avian orders (Passeriformes [songbirds, e.g. sparrows], Trochiiformes [hummingbirds], and Psittaciformes [parrots]). • In other orders songs can be complex, but are hard-wired rather than learned.

48. Ultimate explanations for birdsong • Based on the phylogenetic relationships of the groups song learning may have evolved independently in each group or may have been present in the groups’ common ancestor, but been lost in ancestors of the non-learning orders. • Both hypotheses are equally plausible as only three independent losses of the trait would have been required.

49. Ultimate explanations for birdsong • However, the song control systems in the brains of the three groups are very similar, which suggests song learning was most likely derived from one common ancestor and lost independently by several groups.