1. Hormones And Neurobiology
Chapter 3:
Hormones And Neurobiology
Proximate and Ultimate Perspectives
Hormones and Proximate Causation
Neurobiology and Behavior

3. Proximate and Ultimate Perspectives
Proximate: here and now
Ultimate: then, now and why
House Finches (Geoff Hill, Auburn University)
Plumage coloration
Sexual dimorphism
Males are brightly colored
Females are not
FIGURE 3.1. Natural variation. Significant natural variation exists in house finch coloration. This variation set the stage for Hill’s work on proximate and ultimate questions related to plumage coloration. (Photo credit: Geoff Hill)

4. Proximate Question: Ultimate Question:
What causes males to be more brightly colored ?
Ultimate Question:
Why does this dimorphism persist over evolutionary time?
FIGURE 3.2. Plumage manipulation. As part of the study on plumage coloration, Geoff Hill artificially brightened (top left photo to top right photo) or lightened (bottom left photo to bottom right photo) the plumage coloration of male house finches. (Photo credit: Geoff Hill)

5. Proximate Question: What causes males to be more brightly colored ?
Carotenoids cause the coloration.
Over 600 compounds
Xanthophylls (contain oxygen)
Carotenes (no oxygen)
Carotenoids absorb green to violet wavelengths
seen as yellow, orange, or red
Animals do not synthesize these compounds (two exceptions spider mites and aphids)
They are acquired in the diet.
FIGURE 3.2. Plumage manipulation. As part of the study on plumage coloration, Geoff Hill artificially brightened (top left photo to top right photo) or lightened (bottom left photo to bottom right photo) the plumage coloration of male house finches. (Photo credit: Geoff Hill)

6. Proximate Question: What causes males to be more brightly colored ?
So male House Finches must eat more carotenoids than females.
Across populations, differential availability of carotenoid in food seems to explain the variation.
1. Females fed high carotenoid diets were more colorful than females fed low carotenoid diets.
2. In populations where there higher carotenoid levels in the diet, females tend to be more colorful.
Within populations, males seems to forage differently from females.
1. Males actively seek and eat high carotenoid food, females will eat almost any diet.
2. Males have more colorful plumage directly related to their foraging activity.
FIGURE 3.2. Plumage manipulation. As part of the study on plumage coloration, Geoff Hill artificially brightened (top left photo to top right photo) or lightened (bottom left photo to bottom right photo) the plumage coloration of male house finches. (Photo credit: Geoff Hill)

7. Proximate Question: What causes males to be more brightly colored ?
This just in…
Matthew B. Toomey, Ricardo J. Lopes, Pedro M. Araújo, James D. Johnson, Małgorzata A. Gazda, Sandra Afonso, Paulo G. Mota, Rebecca E. Koch, Geoffrey E. Hill, Joseph C. Corbo, and Miguel Carneiro
High-density lipoprotein receptor SCARB1 is required for carotenoid coloration in birds
PNAS 2017 : v
The gene SCARB1regulates the uptake of carotenoids in the gut of birds!
Lopes, R. L., J. D. Johnson, M. B. B Toomey, S. M. Ferreira, J. Melo-Ferreira, L. Andersson, G. E. Hill*, J. C. Corbo*, and M. C. Carneiro* The redness gene in birds. Current Biology
FIGURE 3.2. Plumage manipulation. As part of the study on plumage coloration, Geoff Hill artificially brightened (top left photo to top right photo) or lightened (bottom left photo to bottom right photo) the plumage coloration of male house finches. (Photo credit: Geoff Hill)

8. Proximate Question: What causes males to be more brightly colored ?
and
Lopes, R. L., J. D. Johnson, M. B. B Toomey, S. M. Ferreira, J. Melo-Ferreira, L. Andersson, G. E. Hill, J. C. Corbo*, and M. C. Carneiro The redness gene in birds. Current Biology
There is an enzyme (ketolase) that allows birds to convert yellow dietary carotenoids to red carotenoids used for ornamental feather coloration. (This ketolase is a cytochrome P450)
FIGURE 3.2. Plumage manipulation. As part of the study on plumage coloration, Geoff Hill artificially brightened (top left photo to top right photo) or lightened (bottom left photo to bottom right photo) the plumage coloration of male house finches. (Photo credit: Geoff Hill)

9. Ultimate Question:
Why does this dimorphism persist over evolutionary time?
Why do males search for high carotenoid foods?
What are the benefits to the males how do this?
Hill’s color manipulation studies in House Finches (1990 through 1993)

10. Using hair dye and bleach he altered male plumage coloration
FIGURE 3.2. Plumage manipulation. As part of the study on plumage coloration, Geoff Hill artificially brightened (top left photo to top right photo) or lightened (bottom left photo to bottom right photo) the plumage coloration of male house finches. (Photo credit: Geoff Hill)
Using hair dye and bleach he altered male plumage coloration
(Hill, 1991)

11. The males were released into the population and the number of mate pairings and time to pairing were measured.
100% of brightened males were paired in 12 days
(Hill, 1991)
TABLE 3.1. Plumage manipulation.

12. More “ultimate” questions:
Why do females prefer (choose) the more colorful males?
Disease resistance and parasite load (Hamilton and Zuk, 1982; Hill and farmer, 2005)
FIGURE 3.3. Plumage coloration and disease. (A) The rate at which birds recovered from Mycoplasma gallicepticum, which causes eye swelling, was linked with their plumage coloration. Birds with more red coloration recovered more quickly (in later phases of the experiment) than birds with more yellow coloration. (B) Individuals with redder plumage carried fewer feather-degrading bacteria. (From G. Hill and Farmer, 2005; Shawkey et al., 2009)

13. More “ultimate” questions:
Why do females prefer (choose) the more colorful males?
More colorful males make better fathers. Parental investment increased in more colorful males.
(Hill, 1991)
and… More colorful males tend to be better foragers and this leads to higher survivorship. And this trait appears to be heritable.
FIGURE 3.4. Plumage, feeding, and between generation correlation. (A) The relationship between male plumage and the rate of feeding offspring. (B) A significant positive relationship exists between father and son plumage brightness scores in house finches. (From G. Hill, 1991)

14. Hormones and Proximate Causation
FIGURE 3.5. Endocrine cells and target cells. A schematic of how endocrine cells work and how hormones eventually affect target cells. Enzymes in the Golgi apparatus process proteins into hormone molecules and package them inside secretory vesicles. These vesicles fuse with the cell membrane and release the hormone molecules into the bloodstream. The hormone molecules travel through the bloodstream until they reach the receptor sites of the target cell, where they bond and initiate a series of interactions. Here we see the schematic for a membranebound receptor, which is generally part of a peptide hormone system. Steroid hormones often pass right through a membrane to bind to receptors. (Adapted from R. Nelson, 2005)

15. Effects of Ecotourism on stress in Magellanic Penguins
FIGURE 3.6. Magellanic Penguins. Field endocrinology experiments on Magellanic penguin behavior have shed light on issues of conservation biology. (Photo credit: Copyright © Chappell, Mark/Animals Animals—All rights reserved.)

16. Many bird species breed during the spring and early summer, and changes in day length are an excellent cue for seasonal change. As day length changes, it affects circulating levels of testosterone (T). Increases in T increase the probability that males are aggressive toward one another (to gain access to females), guard their mates, build nests, and defend their broods. (From B. Walker et al., 2005)
FIGURE 3.8. Day length, hormones, and behavior. Many bird species breed during the spring and summer, and changes in day length are an excellent cue for seasonal change. As day length changes, it affects circulating levels of testosterone (T). Increases in T increase the probability that males are aggressive toward one another (to gain access to females), guard their mates, build nests, and defend their broods. (From B. Walker et al., 2005)

17. How the endocrine system integrates sensory input and output
FIGURE 3.9. Complex effects of hormones. Hormones can affect input systems (sensory systems such as those for smell, sight, or hearing), central nervous system functions (processing), and output systems (for example, effectors such as muscles controlling movement). (Adapted from R. Nelson, 2005)

18. FIGURE 3. 10. Testosterone (T) and aggression feedback loop
FIGURE Testosterone (T) and aggression feedback loop. A positive feedback loop exists between levels of T and probability of winning a fight. High levels of T increase the probability of winning, whereas winning further increases circulating levels of T.

19. Effects of circulating testosterone during development
Intrauterine position in mice
FIGURE Intrauterine position. Males surrounded by two females in utero act relatively “feminized,” whereas females surrounded by two males act relatively “masculinized.” These behavioral differences are typically a result of differential exposure to hormones in utero. 1M = adjacent to one male; 2M = surrounded by two males; 2F = surrounded by two females. (From vom Saal, 1989)

20. Long-term effects of intrauterine position
In Mongolian Gerbils
2M males had significantly higher lifetime testosterone levels than 2F males
2M males sired more pups than 2F males
2M males were more aggressive than 2F males
2M males mounted faster, ejaculated sooner
2F males spent more time with offspring
FIGURE Helping in male Mongolian gerbils. Male helping behavior as a function of prior intrauterine position has been examined in Mongolian gerbils. (Photo credit: Julian Barker)

21. FIGURE 3. 14. In utero position and subsequent parental behavior
FIGURE In utero position and subsequent parental behavior. Males that were surrounded by two males in utero (2M males) provided less parental care when they matured than did males that were surrounded by two females in utero (2F males). (From M. Clark et al., 1998)

22. FIGURE 3. 15. Testosterone and male parental care
FIGURE Testosterone and male parental care. When male Mongolian gerbils were castrated, they spent more time with pups than did “sham” castrated males that had undergone a similar operation but were not actually castrated. (From M. Clark et al., 2004)

23. Oxytocin and Vasopressin
FIGURE Evolutionary history of vasopressin and oxytocin. Note the similarity in amino acid structure between all the neurohormones on this phylogenetic tree. (From Donaldson and Young, 2008)

24. FIGURE 3. 17. Vasopressin receptors in prairie and meadow voles
FIGURE Vasopressin receptors in prairie and meadow voles. Vasopressin receptors in both species are concentrated in the ventral pallidum (VP) area of the brain. (From Donaldson and Young, 2008)

25. Hormones and Honeybee Foraging Proximate questions
FIGURE Honeybee foraging. The proximate underpinnings of foraging behavior in honeybees have been studied in depth. (Photo credit: George D. Lepp/ Corbis)

26. In bees, hormones regulate development and determine foraging behavior
Juvenile hormone determines shift to foraging
Octopamine increases foraging
FIGURE Bee surgery. To examine the effect of juvenile hormone (JH III) in honeybee foraging, Sullivan removed the corpus allatum—the gland that produces this hormone. The inset shows a view through the incision. (Adapted from J. Sullivan et al., 2000)

27. FIGURE 3. 20. Comparing vertebrate and invertebrate systems
FIGURE Comparing vertebrate and invertebrate systems. A comparison of the vertebrate adrenal system with the invertebrate octopamine system. (Adapted from Roeder, 1999)

28. Neurobiology How nerves work
FIGURE Nerve cell. Information is collected by dendrites (which often have dendritic spines projecting off their surfaces), conducted along an axon, and transmitted from the axon terminals across the synaptic gap to the dendrites of neighboring cells.

29. FIGURE Brain scans. Ten male rats were presented with either their female cage mate or their female cage mate and a male intruder. Different activity patterns in different parts of the brain were detected (red indicates activity). (From Ferris et al., 2008)

30. Vocalization in Plainfin Midshipman
FIGURE Vocal fish. In plainfin midshipman, some male types produce vocalizations while others do not. (A) The two smaller fish on the ends are type II sneaker males (that do not sing), whereas the fish that is second from the left is a “singing” type I parental male. (B) A type I male in his nest with his brood attached to the rocks. (Photo credits: Andrew Bass)

31. TABLE 3.2. Traits of type I and type II males.

32. FIGURE 3. 31. Sonic muscles and vocalization
FIGURE Sonic muscles and vocalization. (A) The vocal organ of the plainfin midshipman is made up of a pair of sonic muscles attached to the walls of the swim bladder. (B) Sonic muscles of type I males are well developed in comparison with muscles from (C) type II males. (From Bass, 1996, p. 357)

33. Proximate Functions of Sleep Behavior
FIGURE Sleeping apparatus. This experimental housing unit was employed to record eye state and electrophysiology of four mallard ducks. Eight infrared cameras were used to allow the movement of each eye of each mallard to be recorded. Birds on the extreme left and right were considered to be on the edges of the group. (From Rattenborg et al., 1999a)

34. FIGURE 3. 33. Unihemispheric sleep
FIGURE Unihemispheric sleep. (A) Percentage of time ducks spent with one eye closed or both eyes closed as a function of position in the group (at the group’s center or on its edge). (B) When ducks were at the edge of a group and had one eye open, they spent much more time looking away from the group’s center than when they had one eye open and were at the center of the group. (From Rattenborg et al., 1999a)

35. FIGURE 3. 34. Sleep in aquatic mammals
FIGURE Sleep in aquatic mammals. In some aquatic mammals, like the fur seal, unihemispheric sleep is thought to allow individuals to swim to the surface and breathe during sleep. Here the fur seal is shown sleeping on its left side as its left hemisphere sleeps. The right hemisphere remains awake, controlling paddling of the left flipper and keeping its nostrils above water. When the right hemisphere sleeps, the left hemisphere controls paddling of the right fl ipper and breathing. (From Rattenborg et al., 2000)

36. FIGURE 3. 35. Sleep in dolphins
FIGURE Sleep in dolphins. EEG activity was measured in dolphins during unihemispheric sleep. (From Mukhametov et al., 1988)