1. Reaction norms and genetic assimilation

2. Two individuals of a single clone of the Asian and African water flea, Daphnia lumholtzi. The individual on the left was exposed to chemical cues from predaceous fish (induced); the individual on the right was not (control).

3. Sundew: green & red morphs H 1 : Morphs have different genotypes. H 2 : Morphs have same genotype but developed in different environments. If H 2, why should the plant have the capability of producing different forms?

4. 3.3 Two morphs of Araschnia levana, the European map butterfly

5. What are the questions? Can flexibility be an adaptation? Can flexibility be an adaptation? What is phenotypic plasticity? What is phenotypic plasticity? How does p.-p. contrast with canalization? How does p.-p. contrast with canalization? What aspects of phenotypic plasticity are heritable? What aspects of phenotypic plasticity are heritable? How can we test the hypothesis of adaptive plasticity? How can we test the hypothesis of adaptive plasticity?

6. Phenotypic plasticity defined environment-dependent phenotypic expression environment-dependent phenotypic expression identical genotypes are exposed to different environments identical genotypes are exposed to different environments traits of interest measured traits of interest measured

7. Antonym: canalization a developmental process that produces the same phenotype in spite of environmental variability (= homeostasis) a developmental process that produces the same phenotype in spite of environmental variability (= homeostasis) reduces the effect of environmental “noise” reduces the effect of environmental “noise” variability in a trait in a population represents a balance between plasticity and canalization variability in a trait in a population represents a balance between plasticity and canalization

8. Measuring phenotypic plasticity Norm of Reaction Norm of Reaction Different phenotypes produced by the same genotype in different environments Different phenotypes produced by the same genotype in different environments “X- axis” represents range of environmental conditions “X- axis” represents range of environmental conditions “Y-axis” represents the resulting phenotype “Y-axis” represents the resulting phenotype

9. Forms of Norms of Reaction Red lines indicate optimal reactions Arrows indicate optimal phenotypes for each environment

10. Norm of Reaction curves for biomass allocation in Polygonum From Sultan, S. E. 2003. Phenotypic plasticity in plants: a case study in ecological development. Evolution & Development 5:25-33.

11. Norms of reaction for leaf area (morphological plasticity)

12. Norms of reaction for reproductive plasticity (lifetime output)

13. Is phenotypic plasticity an adaptation? It depends It depends Are patterns heritable? Are patterns heritable? Do “plastic” genotypes have more success than “canalized” genotypes? Do “plastic” genotypes have more success than “canalized” genotypes? Nijhout, H. F. 2003. Development and evolution of adaptive polyphenisms. Evolution & Development 5: 9-18. Nijhout, H. F. 2003. Development and evolution of adaptive polyphenisms. Evolution & Development 5: 9-18.

14. What is a “polyphenism”? Two or more discrete alternative phenotypes, without intermediate forms Two or more discrete alternative phenotypes, without intermediate forms

15. Why, in nature, are there just 2 forms?

16. 3.4 Two morphs of Nemoria arizonaria

17. Hormonal & developmental programs influence polyphenism: a heritable mechanism

18. Correlated characters in beetles: size & mating tactics (variation in success)

19. Other examples of polyphenism castes of social insects (Nature 26 Oct 2006) castes of social insects (Nature 26 Oct 2006) alternative seasonal form of insects alternative seasonal form of insects alternative leaf forms in plants alternative leaf forms in plants predator-induced polymorphism in cladocerans polymorphism in migratory behavior of locusts predator-induced polymorphism in cladocerans polymorphism in migratory behavior of locusts sedentary vs. dispersal morphs of aphids & other animals sedentary vs. dispersal morphs of aphids & other animals

20. Is Polyphenism adaptive? - tadpoles Relyea, R. A. 2005. The heritability of inducible defenses in tadpoles. J. Evol. Biol. 18: 856-866. Relyea, R. A. 2005. The heritability of inducible defenses in tadpoles. J. Evol. Biol. 18: 856-866.

21. Tadpole norms of reaction

22. Heritability of Plasticity

23. What is different about phenotypic plasticity as an adaptation? Compared to selection on a continuous trait influenced by additive genetic effects? Compared to selection on a continuous trait influenced by additive genetic effects? Consider rate of response Consider rate of response in context of rate of environmental change in context of rate of environmental change in context of shifting gene frequencies in context of shifting gene frequencies As a response to spatial heterogeneity? As a response to spatial heterogeneity?

24. Spea hammondiiScaphiopus couchii Pelobates syriacusPelodytes punctatus

25. Genetic assimilation: the work of Schmalhausen and Waddington and an introduction to systems biology

26. Seen as vague competitors… Schmalhausen (1884-1963)Waddington (1905-1975)

27. The role of selection in evolution Schmalhausen noted that there are two opposing tendencies in evolution: selection, which tends to lead to phenotypic change; and heredity, which tends to lead to phenotypic conservation. He tried to come up with a synthetic theory that reconciled these two forces. Schmalhausen noted that there are two opposing tendencies in evolution: selection, which tends to lead to phenotypic change; and heredity, which tends to lead to phenotypic conservation. He tried to come up with a synthetic theory that reconciled these two forces.

28. Mutations and environment For example, it is wrong to think about mutations producing a definite phenotypic effect: For example, it is wrong to think about mutations producing a definite phenotypic effect:

29. E.g. The case of vestigial FemaleMale

30. Female

31. Shows that the effect of mutations is both variable and often dependent on the environment Shows that the effect of mutations is both variable and often dependent on the environment Basis for this thermosensitivity has been further examined. Basis for this thermosensitivity has been further examined. In the wildtype, the amount of vg transcribed stays constant with temperature. So this suggests that low levels of normal vg are what trigger the temperature dependency of the system. In the wildtype, the amount of vg transcribed stays constant with temperature. So this suggests that low levels of normal vg are what trigger the temperature dependency of the system.

32. But mutations not needed! Introduces the concept of “phenocopies”: environmentally induced morphologies that mimic mutations. Introduces the concept of “phenocopies”: environmentally induced morphologies that mimic mutations.

33. Temperature shocking Aglais urticae produces phenocopies of geographic variants. (A) Usual central European variant; (B) heat-shock phenocopy resembling Sardinian form; (C) a Sardinian form of the species. (After Goldschmidt 1938.)

34. The Baldwin Effect “A New Factor in Evolution” - Baldwin, 1896 “A New Factor in Evolution” - Baldwin, 1896 Argued that behaviour could alter selective regime. In time, selection would reinforce that behaviour until it became instinctual Argued that behaviour could alter selective regime. In time, selection would reinforce that behaviour until it became instinctual Note that this effect converts phenotypic plasticity into genetically determined behaviour! Note that this effect converts phenotypic plasticity into genetically determined behaviour! Has always been controversial Has always been controversial

35. The classic example of ostriches

36. How did the ostrich get its calluses?

37. Calluses form where the ostrich’s skin is under pressure by contact with the ground when it sits. Calluses form where the ostrich’s skin is under pressure by contact with the ground when it sits. But ostriches actually hatch with such calluses! But ostriches actually hatch with such calluses!

39. Baldwin’s explanation When ostriches sit on the ground, the pressure on the skin causes calluses to form. When ostriches sit on the ground, the pressure on the skin causes calluses to form. However, this reaction will be variable, and under genetic control. However, this reaction will be variable, and under genetic control. Hence, those ostriches that best form calluses will be selected for. Hence, those ostriches that best form calluses will be selected for.

40. Baldwin’s explanation part II In time, assuming a constant environment, the population as a whole will form calluses more reliably and with less stimulus. In time, assuming a constant environment, the population as a whole will form calluses more reliably and with less stimulus. And in time, why need any stimulus at all? And in time, why need any stimulus at all? Similar arguments are ongoing about the origin of language in humans. Similar arguments are ongoing about the origin of language in humans.

41. Baldwin’s work was theoretical, but Waddington provided some experimental evidence for just such an effect, which he called “genetic assimilation”, and which Schmalhausen called “stabilising selection”. Also controversial. Baldwin’s work was theoretical, but Waddington provided some experimental evidence for just such an effect, which he called “genetic assimilation”, and which Schmalhausen called “stabilising selection”. Also controversial.

42. Waddington’s Fruitfly experiments Waddington took a population of Drosophila and dumped their eggs in ether. Waddington took a population of Drosophila and dumped their eggs in ether. Rather surprisingly, a proportion of the subsequent adult flies produced a bithoracic phenotype Rather surprisingly, a proportion of the subsequent adult flies produced a bithoracic phenotype This is of course a phenocopy of a well- known set of homeotic mutations This is of course a phenocopy of a well- known set of homeotic mutations

43. Actually a set of homeotic mutations!

44. Waddingtonian fruit fly. Note he has removed anterior wings for clarity!

45. Selection on Waddington’s flies Waddington selected the flies that produced the best attempts at wings and bred from them. Of course, their offspring produced normal wings. Waddington selected the flies that produced the best attempts at wings and bred from them. Of course, their offspring produced normal wings. But he also dumped the eggs in ether, and again the population produced some bithorax flies. But he also dumped the eggs in ether, and again the population produced some bithorax flies.

46. Continued selection He carried on doing this, and noted two changes in the population: He carried on doing this, and noted two changes in the population: I) On average, the flies produced better wings. I) On average, the flies produced better wings. II) More of them did so. II) More of them did so. With some complications, on the 29th generation, flies started producing transformed halteres even without treatment! With some complications, on the 29th generation, flies started producing transformed halteres even without treatment!

48. Even further selection… By breeding from the bithoracic flies in the 29th population, Waddington managed to eventually fix the phenotype: all the flies produced it in the population without ether treatment. By breeding from the bithoracic flies in the 29th population, Waddington managed to eventually fix the phenotype: all the flies produced it in the population without ether treatment. Conversely, the down selection experiments produced the opposite effect: they produced flies that did not respond to ether treatment. Conversely, the down selection experiments produced the opposite effect: they produced flies that did not respond to ether treatment.

49. Another experiment: cross-veins in wings Waddington also showed that when fly eggs were heat shocked, a certain wing character appeared, that could also be selected for and would eventually appear without any heat shocking. Waddington also showed that when fly eggs were heat shocked, a certain wing character appeared, that could also be selected for and would eventually appear without any heat shocking.

50. Reactions to G.A. ‘... [genetic assimilation] is an interesting but, I would judge, relatively minor outcome of the [synthetic] theory’ (Simpson,1953) ‘It represents merely a degeneration of a part of an original adaptation’ (Williams, 1966) ‘A baroque hypothesis’ (Orr, 1999).

51. The genetics of genetic assimilation! Hsp90 (heat shock protein): the chaperone molecule Hsp90 (heat shock protein): the chaperone molecule Plays a role in stabilising several unstable developmental pathways, for example, steroid hormone receptors. Plays a role in stabilising several unstable developmental pathways, for example, steroid hormone receptors. Its function can be knocked down or out using the drug geldanamycin, or by mutations Its function can be knocked down or out using the drug geldanamycin, or by mutations Rutherford and Lindquist found that when this was done, a variety of abnormalities appeared in various systems. These could be selected for and would eventually appear no matter what the Hsp90 levels were. Rutherford and Lindquist found that when this was done, a variety of abnormalities appeared in various systems. These could be selected for and would eventually appear no matter what the Hsp90 levels were.

52. C after selection…

54. Can one have “internal assimiliation”? Budd (1999, 2006) suggested that a process analogous to genetic assimilation could take place within the genome too. Budd (1999, 2006) suggested that a process analogous to genetic assimilation could take place within the genome too. May help explain how deep developmental shifts can take place without developmental disasters! May help explain how deep developmental shifts can take place without developmental disasters!

55. Example: bicoid, nanos In Drosophila, maternal mRNA is deposited in the egg from the nurse cells at the anterior. Bicoid stays put; nanos is transported to the posterior. In Drosophila, maternal mRNA is deposited in the egg from the nurse cells at the anterior. Bicoid stays put; nanos is transported to the posterior. The mRNA is then translated, and a double gradient is set up. This acts as the framework to establish the A-P axis along which future differentiation (segmentation, hox genes etc) takes place. The mRNA is then translated, and a double gradient is set up. This acts as the framework to establish the A-P axis along which future differentiation (segmentation, hox genes etc) takes place.

56. Bicoid and nanos regulate the translation of two other maternal genes; hunchback and caudal (nanos inhibits hunchback).

57. Hunchback seems to be a mistake As all nanos does is repress it. If you knock out both, flies develop normally! As all nanos does is repress it. If you knock out both, flies develop normally!

58. What about bicoid? Its sequence is similar to Hox3! Its sequence is similar to Hox3! It is only found in the higher dipterans!

59. Bicoid-nanos is derived. Higher dipterans are very “long germ band”. Ancestral AP patterning very different

60. Example two: “homeotic takeover” How do Hox gene expression patterns evolve? How do Hox gene expression patterns evolve?

61. Gellon and McGinnis - hopeful monsters!

62. Selective pressure? Budd 1999

63. But there is another way… …of looking at this, which is more subversive. …of looking at this, which is more subversive. Development can be seen as a cooperation between genes and environment, of variable influence of both. I will discuss extreme “environment” issues tomorrow. Development can be seen as a cooperation between genes and environment, of variable influence of both. I will discuss extreme “environment” issues tomorrow.

64. Environmental stress… …leads to altered developmental outcomes. …leads to altered developmental outcomes. Through time, and through selection, there is true genetic alteration of development too (not necessarily involving mutation, of course!). Through time, and through selection, there is true genetic alteration of development too (not necessarily involving mutation, of course!). Plan A (environmental stress plus development 1) is replaced by Plan B (development 2, without environmental stress). Plan A (environmental stress plus development 1) is replaced by Plan B (development 2, without environmental stress). Thus, the same morphologies in Plan A and Plan B have different genetic backgrounds - Roth’s “genetic piracy”; Weiss and Fullerton’s “phenogenetic drift”. Thus, the same morphologies in Plan A and Plan B have different genetic backgrounds - Roth’s “genetic piracy”; Weiss and Fullerton’s “phenogenetic drift”.

65. Gene pirates and selfish genes All this implies a systems approach to evolution. Selection truly acts on the phenotype; any genotype that generates a favoured phenotype under particular conditions will be selected for; and one can trace, via genetic assimilation experiments, precisely this process. All this implies a systems approach to evolution. Selection truly acts on the phenotype; any genotype that generates a favoured phenotype under particular conditions will be selected for; and one can trace, via genetic assimilation experiments, precisely this process.

66. Gene pirates and selfish genes (ii) And if within a population, several equivalent genotypes persist, they can shift via drift. And if within a population, several equivalent genotypes persist, they can shift via drift. Implication is that selection acts at the whole organism level, not at the genetic level. In this way of thinking about things, genetic networks are the slaves of the phenotype, not the other way round. Implication is that selection acts at the whole organism level, not at the genetic level. In this way of thinking about things, genetic networks are the slaves of the phenotype, not the other way round. Strict genetic encoding may not be the only repository of information that is stable enough to enable selection to take place. Strict genetic encoding may not be the only repository of information that is stable enough to enable selection to take place.

67. Remember heterochrony May be environmentally induced (e.g. temperature affecting speed of development) - could become genetically assimilated? May be environmentally induced (e.g. temperature affecting speed of development) - could become genetically assimilated? Cf Island dwarfism Cf Island dwarfism

68. 23.20 Co-option of signal transduction pathways in the formation of butterfly eyespots