1. Chapter 3

2. Development of Behavior  Development is an interactive process in which the genes are turned on and off both in response to environmental change and simultaneously creating change.  This demonstrated by changes in behavior shown by honeybees over the course of their lives.

3. Development of Behavior  Honeybees when they emerge as adults first work at cleaning cells then as they age they shift to other tasks.  Eventually at about age 3 weeks they begin foraging outside the hive.

5. Development of Behavior  As the bee goes through these changes in behavior it appears that predictable changes in the genes being actively expressed occur.  Microarray technology makes it possible to scan for activity levels of many genes by detecting mRNA made when genes are turned on.

6. Development of Behavior  Comparisons of arrays of nurse and forager bees shows substantial differences in genes turned on at each stage.

7. (YN= young nurses, OF = older foragers)

8. Development of Behavior  Transition to worker role appears to be strongly influenced by level of a hormone called juvenile hormone, which is produced by a gene.  The juvenile hormone gene turns on apparently in response to activity of other genes during 1 st three weeks of adulthood, but can also be turned on in response to conditions in the hive.

9. Development of Behavior  If colonies are artificially made up of only young workers some become foragers much sooner and others remain as nurse bees much longer.  It may be social encounters that stimulate these changes.  Lack of encounters with older foragers appears to hasten nurse bees transition to forager role.

10. Development of Behavior  Adding numbers of older bees to hives that contain only young bees reduces the number of young bees that become foragers.  In contrast, adding more young bees does not slow rate at which young bees become foragers.

12. Development of Behavior  Inhibiting agent believed to be a chemical called ethyl oleate that foragers manufacture and store in their crop.  When foragers transfer food to nurse bees they transfer the chemical, which slows the nurses transition to foragers.

13. Development of Behavior  In honeybees, therefore, sequence of behavioral changes is determined by continuous interactions between genes and both chemical and social environments.

14. Nature vs Nurture Debate  Nature: genetic contribution to behavior.  Nurture: environmental contribution to molding behavior.  There is a false dichotomy in popular discussions in which traits are considered to be genetically or environmentally determined.

15. Nature vs Nurture Debate  In reality, all traits are the product of gene-environment interactions.  As we saw in the process of song learning there is considerable gene-environment interaction.

16. Nature vs Nurture Debate  Environmental or genetic differences among individuals can lead to differences in development and finally differences in behavior.

17. What causes individuals to develop differently?  Environmental differences and behavioral differences.  Many behavioral differences result from differences in experience.  For example, marsh tits fed whole sunflower seeds, which they can hide and later retrieve, develop a larger hippocampus in their brain than birds fed only powdered sunflower seeds. Practice of storing and retrieving seeds alters brain development.

18. Learning of nestmates in Polistes wasps  Polistes wasps learn to identify the smell of their natal nest and tolerate individuals that smell like the nest (whether or not they are relatives).  Individuals with a different smell are attacked. Differences in how wasps behave towards each other thus are based on the smells they learned when young.

19.  Similar discrimination between individuals reared together versus apart has been shown in Belding’s Ground Squirrels.  Non-relatives reared together act nicely towards each other. However, relatives reared apart also act nicely towards each other.

20.  Ground squirrels apparently learn what they themselves smell like and use this information to evaluate their relatedness to other individuals.  Trials in which squirrels provided with cubes smeared with dorsal gland secretions of other individuals respond more strongly to those of non-relatives and discriminate between different degrees of relatedness.

22. Genetic differences and behavioral differences  Breeding experiments can show whether behavioral differences between populations have a genetic basis.

23. Funnel Web Spiders  Spiders in different habitats differ in their speed of reaction to food being caught in their webs.  Streamside spiders react slowly.  Desert grassland spiders react quickly.  Is difference largely environmental or genetic?

24. Funnel Web Spiders  Spiders bred in lab.  Offspring of both populations kept equally well fed. Then offered food.  Desert spider reaction time: 3s.  Streamside spider reaction time: 60s.  Most of the difference in behavior apparently due to genetic differences between populations.

25. Migratory behavior of European Blackcaps

26.  Blackcaps are small European warblers, most of which migrate to Africa to winter. However, some spend the winter in Britain.  What causes this difference in behavior?

27. Migratory behavior of European Blackcaps  Peter Berthold caught wintering blackcaps in Britain.  He then bred these birds in central Germany in outdoor cages.

28. Migratory behavior of European Blackcaps  In fall Berthold looked at migratory direction selected by birds.  Used an Emlen funnel to record orientation.

29. Emlen Funnel

30. Blackcaps oriented in a westerly direction. Conclusion? British birds from where?

31. Migratory behavior of European Blackcaps  Based on orientation birds not from Scandinavia or northern Britain.  Birds probably from due east of Britain Belgium or Germany.

32. Migratory behavior of European Blackcaps  Could environmental influences be responsible?  Perhaps, just being in Germany causes westward orientation.

33. Migratory behavior of European Blackcaps  To check birds from SW Germany were bred in captivity.  Migratory orientation was checked.

34. SW German birds oriented southwest.

35. Migratory behavior of European Blackcaps  Differences in orientation between populations largely determined by genetic differences.  Southwest German birds migrate SW traveling west of the Mediterranean via Spain.

37. Migratory behavior of European Blackcaps  Andreas Helbig has shown that Blackcaps from Austria orient southeast.  They travel east of the Mediterranean via Turkey and Israel.

39. Migratory behavior of European Blackcaps  Helbig crossed birds from Austria with birds from southwest Germany.  What direction did they orient?

40. Mean orientation of offspring south. Inner ring Adults. Outer ring Offspring.

41. Migratory behavior of European Blackcaps  Due south is a poor choice. Requires bird to cross the Alps and the make a long sea crossing over the Mediterranean.

43. Single gene effects on development  In theory a single gene difference could be responsible for difference in orientation on different Blackcap populations.  Note a single gene does not encode migratory choices, but a change in a single gene can result in many gene-environment effects and ultimately produce a large behavioral difference.

44. Rovers move a lot when feeding. Sitters move very little. Sitter Rover Two strains of Drosophila differ in larval foraging behavior.

45. Rover/sitter behavior in Drosophila  When the two strains were crossed in the F1 generation all of the larvae were rovers.  A cross of members of the F1 generation produced a 3:1 ratio of rovers to sitters.

47. Rover/sitter behavior in Drosophila  One gene appears to be responsible for difference between phenotypes.  The rover allele is dominant and the sitter allele is recessive. Gene that affects rover/sitter behavior affects the olfactory system and may affect fly’s ability to sense its environment.

48. Rover/sitter behavior in Drosophila  Many other single gene effects in Drosophila.  E.g. Stuck: males don’t dismount after normal 20 minutes of copulation.  Coitus interruptus: male copulates for only 10 minutes.

49. Single gene examples from lab mice   Mice homozygous for allele for defective form of  calmodulin kinase have poor learning ability.

50. Single gene examples from lab mice  Mouse placed in water-filled container.  Submerged platform available for rest.  Normal and mutant mice tested with platform in random locations and original testing position.  Time to find platform measured.

51. When platform kept in same location as in training trials wild-type mice found platform much faster than mutant mice, but not if position of platform was randomized.

52. fosB gene  In normal mice sniffing and touching pups causes changes in female’s brain that prompt her to care for pups.  Mice homozygous for inactive fosB gene ignore their pups.  Funtional fosB gene usually activated in hypothalamus by smell of newborn pups.

53. Pups Female with active fosB Female with inactive fosB

54. Oxt gene   Mice missing Oxt gene cannot produce oxytocin.   Mutant male mice cannot remember scent of females they recently interacted with.

56. A gene “for”  Remember that one gene does not code for a behavior.  One gene codes for one enzyme.  Bit a change in one enzyme can alter numerous gene-environment interactions and produce a detectable difference in the phenotype.

57. A gene “for”  The phrase “a gene for” some behavior is shorthand for: a change in the gene leads to a change in behavior.  All else being equal, a change in a gene can result in a detectable change in a phenotype.

58. Evolution and behavioral development Garter Snake

59. In California, coastal and inland populations of garter snakes differ in diet.

60. Coastal garter snakes feed on banana slugs.

61. Inland populations eat other foods e.g. fish and frogs.

62.  Is there a genetic basis to the behavioral differences in diet preference?

63. Steve Arnold studied populations to see if there were genetic differences between them. Brought pregnant females into lab and reared babies in isolation. Offered slug pieces to snakes.

64. Inland snakes usually ignored slugs, coastal snakes usually ate it.

65. Then tested newborn snakes on response to odors. Offered snakes flavored cotton swabs, counted number of tongue flicks made.

66. Coastal individuals responded much more strongly to slug odor.

67. Arnold carried out heritability studies. Found little variation within either population. Preference for slugs within a population largely fixed.

68. Crosses between populations produced individuals with wide variation in response to slugs. Suggests differences between populations have strong genetic component.

69. What is evolutionary basis for difference between populations? Advantage to slug eating on coast is obvious. Rare gene for eating slugs would spread rapidly.

70. Artificial selection and behavioral evolution  Nest building in mice.  In starting population mice used 13-18 grams of cotton to line their nests.  Carol Lynch selected for “high”, “low” and “control” groups of mice.

71.  After 15 generations amounts of cotton used by mice were: Controls 15g same as original population. Controls 15g same as original population. High 40g High 40g Low 5g Low 5g

73. Other examples of Artificial Selection  William Cade has selectively bred crickets to sing rarely or almost continuously.  In only two generations of artificial selection Pulido et al. showed that the timing of migration in European Blackcaps could be delayed more than a week.

75. Artificial Selection  Artificial selection experiments show that (i) behavior is subject to selection and (ii) populations contain sufficient genetic variability to evolve rapidly.

76. Adaptability of behavioral development  As we have seen the development of behavior such as singing can be strongly influenced by environmental effects.  It is important for development of behavior to be resilient to disturbance so that normal behavior can develop as often as possible.  Process of developmental homeostasis reduces effects of disturbance.

77. Adaptability of behavioral development  Harlow’s “experiments” with Rhesus monkeys showed that rhesus monkeys entirely derived of contact with mothers and “reared” by artificial surrogates gained weight and grew normally but behaviorally developed abnormally (BIG surprise!) and were terrified of other monkeys if exposed to them.

79. Adaptability of behavioral development  However, monkeys given even 15 minutes contact a day with other young monkeys developed essentially normally.

81. Adaptability of behavioral development  As adults, these monkeys interacted normally with others unlike those individuals which had no social contacts as infants, which were withdrawn or very aggressive.

82. Read Dawkins chapters 4 and 5 for next Friday. First exam is Wednesday February 22 nd.

83. Developmental homeostasis in human embryonic development  We saw in studies of songbirds that adult ability to learn and sing complex songs was affected by food deprivation during period of rapid nestling growth.  In humans food deprivation of the mother during pregnancy appears not to have major effects on the fetus’ intelligence.

84. Developmental homeostasis in human embryonic development  Studies of children whose mothers were food deprived during the Nazi transport embargo of Holland in late WWII showed that these children had comparable intelligence scores and rates of mental retardation as children whose mothers were not food deprived.

87. Symmetry and attractiveness  Many organisms are influenced by how symmetrical other individuals are when making mate choices.  Asymmetries are believed to be caused by problems in development and symmetry thus signals an ability to overcome developmental challenges.

88. Symmetry and attractiveness  There is some evidence that humans include symmetry in their ratings of an individuals’ attractiveness, but data are not conclusive and there is considerable debate.

89.  Female brush-legged wolf spiders, however, are significantly more likely to mate with males whose foreleg hair tufts are symmetrical than those who are not.  Study was carried out using video images of spiders that were identical apart from the digitally manipulated foreleg tufts.

91. Polyphenism  In many species multiple alternative phenotypes occur in the same species (i.e. distinctly different body types occur).  These different phenotypes arise as a result of environmental effects. The environmental influence sends the developing organism down one or another distinct developmental pathway.

92. Developmental flexibility in Tiger Salamnders  Larvae live in ephemeral ponds.  Most follow “normal” development and eat small invertebrates.

93. But some become cannibals (bigger with larger teeth) and eat smaller salamanders.

94. Normal form Cannibal

95. What factors affect decision to become a cannibal?  Ideas?

96. What factors affect decision to become a cannibal?  Relatedness of cannibal to others in pool.  Density of salamanders  Size distribution of salamanders

97.  A salamander surrounded by lots of non- kin can benefit by becoming a cannibal.  By growing faster it can escape from the pond sooner.  Developmental flexibility allows salamander to adjust its development if conditions are suitable, but not otherwise.

98. Behavioral flexibility  Many animals choose among different behavioral phenotypes depending on environmental circumstances.  For example, in many fish males adopt different roles depending on their size and status. Large males defend territories but smaller satellite males act as sneakers darting in and releasing sperm whenever the dominant male mates with a female.

99. Behavioral flexibility in Haplochromis burtoni  In cichlid fish Haplochromis burtoni territorial males are brightly colored and satellite males are dull.  Behavior is related to brain structure.

100. Territorialmale Satellitemale

101. Behavioral flexibility in Haplochromis burtoni  GnRH (gonadotropin releasing hormone) neurons in hypothalamus are 6-8 times larger in territorial males than in satellites.  GnRH neurons stimulate testes development and aggressive behavior.

102. Behavioral flexibility in Haplochromis burtoni  Interestingly, GnRH size is variable.  If male loses territory his neurons shrink and he becomes dull colored.  If territory opens up, male enlarges neurons, switches to aggressive territorial mode

103. Behavioral flexibility in Haplochromis burtoni   Unpredictable social environment favors flexibility in Haplochromis.   Neuronal flexibility allows males to adopt best strategy for conditions.

104. Learning  Learning major element in behavioral flexibility. Ability to make use of experience in adjusting behavior can be selectively very advantageous.

105. Learning in Australian Thynnine wasps  Males search for females based on pheromones they produce.  Orchids attract males using a similar scent.  Orchid mimics female wasps appearance too. When male lands and attempts to mate he gets a surprise.

106. Male tries to mate with “female wasp” on orchid, instead acquires a pollen sac. Female wasp Fake wasp

107. Pollinia on wasp’s back

108. Wasps don’t learn to avoid orchids in general. But, do learn to avoid orchids they have visited before.

109. Learning in Australian Thynnine wasps  What do wasps learn?  Orchid’s location or orchid’s scent?  Speculation: If wasps could learn scent differences how plants benefit from having wasps revisit them?

110. Costs and benefits of learning  For learning and flexible behavior to spread by natural selection, benefits must exceed costs.  Benefits are the ability to exploit the environment more effectively.  What are the costs?

111. Costs and benefits of learning  Costs: Major cost is additional energy required to make/maintain neuronal tissue.

112. Example of cost: West coast marsh wrens sing more songs (100) than east coast marsh wrens (40).

113. Song system in brain weighs 25% more in west coast birds.

114. Costs of large brain in humans  In humans: Brain 2% of body weight.  But requires 15% of body’s oxygen and 20% of energy.  Other costs to large brains in humans?

115. Costs of large brain in humans  Difficulty in giving birth.

116. Behavioral flexibility expensive. Should only evolve when benefit outweighs cost.

117. Clark’s Nutcracker seed-storing specialist.

118. Much better at remembering where Something is located than other crows.

119. Not better at remembering colors, a non- spatial task. Memory skills determined by bird’s needs.

120. Intraspecific variability in learning  Behavioral flexibility does not only differ between species.  In species where males and females experience different selection pressures, differences in learning ability occur.

121. Spatial learning in voles  Male meadow voles are polygynous. Their home ranges are 4X larger than those of females.  Prairie voles are monogamous. Males and females have same size home ranges

122. Spatial learning in voles  Spatial learning abilities of voles was tested in mazes.  Male meadow voles made significantly fewer mistakes than female meadow voles, but there was no difference between the sexes in the performance of male and female prairie voles.

124. Spatial learning in voles  Male meadow voles have a large hippocampus than females and this area in the brain processes spatial information.  However, the enlarged hippocampus only develops during the breeding season.

125. Spatial learning in cowbirds  Female cowbirds parasitize other birds nests. They need to be able to remember nest locations and monitor them over time.

126. Female cowbirds have a larger hippocampus than males. No difference between sexes in related, but non- parasitic grackles and red-winged blackbirds.

127. Operant conditioning  Spatial learning not only behavior that has clearly been shaped by selection.  In operant conditioning (or trial and error learning) an animal learns to associate an action with its consequences.  E.g. a rat pushes a lever and gets a food pellet.

129. Operant conditioning  Usually a behavior and its consequences must be closely linked in time for conditioning to occur.  However, in rats tasting novel foods nausea that occurs several hours after eating a food will be associated with that food, which in future will be avoided.

130. Another example of operant conditioning is that predators learn to recognize noxious prey after tasting them. How does warning coloration benefit animal that is tasted if it is killed?

131. Does operant conditioning occur in humans?