1. 1 Studying Adaptation Evolutionary Analysis of Form and Function Ch. 9

2. 2 Analysis of Adaptation A trait, or integrated suite of traits, that increases the fitness of its possessor is called an adaptation and is said to be adaptive How do we know that a trait is adaptive? The adaptive values of some traits, such as eyes, would not seem to need much explanation The adaptive values of some other traits may be more subtle — and some traits might not be adaptive at all We should be wary of “adaptive storytelling”, accepting plausible hypotheses about adaptation uncritically, and wary of the “adaptationist program” — the idea that all traits are somehow adaptive

3. 3 The giraffe’s neck: an adaptive story An adaptive story –Giraffes evolved long necks (and legs) because taller individuals could browse vegetation that was above the reach of competitors; or because it allowed them to exploit a resource that was not available closer to the ground Prediction –If giraffes are using their height to avoid competition with other browsers or to exploit a preferred resource, they should feed “high”

4. 4 Do giraffes use their height to forage high? (Fig. 9.2)

5. 5 The giraffe’s neck: observations and an alternative hypothesis Giraffes do most of their browsing on vegetation that is at shoulder height Simmons and Scheepers (1996) suggest that long necks evolved for use in male – male contests for access to females –larger males (especially males with thicker necks and more massive horns and skulls) are more likely to win contests with other males –females are more receptive to courtship by males with the stoutest necks, and most massive horns and skulls (= more mating success by larger males?) –this is an argument that long necks evolved through sexual selection: both male – male competition and female choice

6. 6 Male giraffes “neck westling”

7. 7 Neck size and social interactions in giraffes (adapted from Table 9.1) Males in class C are young adults; males in classes A and B are more mature. Class A males are often larger than class B males, but more importantly, class A males have stouter necks, more massive horns, and more heavily armored skulls a. Neck size and male social interactions. These numbers represent observations of one male displacing another from a social group A displaces B, A displaces C, or B displaces C 82 A displaces A, B displaces B, or C displaces C 39 B displaces A, C displaces A, or C displaces B 6 b. Neck size and female choice. These numbers represent male success in obtaining female cooperation in determining female reproductive state SuccessfulUnsuccessful% Successful A bulls 342260.7 B bulls 766155.5 C bulls 458933.6

8. 8 Okapi – the giraffe’s closest living relative (is this what ancestral giraffes looked like?) (do Okapi males fight with their necks and heads?)

9. 9 Caveats Differences among populations or species are not always adaptive –Giraffes from different populations have different spot patterns — are these differences adaptive or accidental? Not every trait, or every use of a trait, is an adaptation –Giraffes do sometimes forage at their full height, but this is not adaptive unless it increases fitness (and even if it does, it’s not necessarily the reason that long necks evolved in the first place) Not every adaptation is perfect –Long necks may help male giraffes get mates, but they make it hard to take a drink

10. 10 Approaches to studying adaptation Experimental manipulation –what happens when a phenotype is experimentally altered? Observational studies –do certain phenotypes have higher fitness than others, or do individuals behave in a way that is consistent with an adaptive expectation? Comparative method –does the same trait evolve repeatedly in related species that share similar environments?

11. 11 Experiment Wing markings and wing-waving display in the tephritid fly Zonosemata (Green et al. 1987) The teprhritid fly Zonosemata vittigera has dark bands on its wings When disturbed, the fly holds out its wings and waves them up and down Seems to mimic the leg waving territorial threat display of some species of jumping spider Hypotheses 1.Not mimicry of jumping spiders 2.Used to deter predators other than jumping spiders 3.Used to deter jumping spiders specifically

12. 12 Experimental treatments for testing the function of wing-waving display by Zonosemata – 1 (Fig. 9.5)

13. 13 Experimental treatments for testing the function of wing-waving display by Zonosemata – 2 (Fig. 9.5)

14. 14 Zonosemata mimic jumping spiders to avoid predation and both components of the mimicry must be present (Fig. 9.6)

15. 15 Observational studies Behavioral thermoregulation in iguanas and garter snakes In ectothermic (cold-blooded) organisms, performance is tied closely to body temperature. In general, there is a relatively narrow temperature range in which endurance, speed, digestive efficiency and other physiological and sensory functions are maximized It would seem to be adaptive, therefore, for animals to regulate their body temperature behaviorally in order to maintain it in or near the zone that maximizes performance

16. 16 Thermoregulation by desert iguanas (Fig. 9.8) ( Huey and Kinsolver, 1989)

17. 17 Behavioral thermoregulation in garter snakes ( Huey et al., 1989) Preferred temperature range in laboratory 28 – 32 ˚C Implanted wild snakes with radio transmitters that made it possible to locate snakes and to record their temperature Snakes maintain body temperature within or very close to their preferred range despite wide fluctuations in environmental temperature Snakes preferentially use micro-environments with temperatures in their preferred range

18. 18 Body temperatures of garter snakes in nature (Fig. 9.9) ( Huey et al., 1989)

19. 19 Environmental temperatures available to garter snakes – 1 (Figs. 9.10a-c) ( Huey et al., 1989)

20. 20 Environmental temperatures available to garter snakes – 2 (Figs. 9.10d-e)

21. 21 Distributions of rocks available to snakes versus rocks chosen by snakes (Table 9.2) (Huey et al., 1989) Thin (< 20 cm) Medium (20 – 40 cm) Thick (> 40 cm) Rocks available to snakes 32.4 %34.6 %33 % Rocks chosen by snakes 7.7 %61.5 %30.8 %

22. 22 The Comparative Method Testis size and social group size in fruit bats and flying foxes (Hosken, 1998) Relative testis size varies among bat species Are large testes an adaptation for sperm competition? Sperm competition can occur when a female mates with two or more males during her fertile period Larger testes may mean more sperm, which may increase chances for successful fertilization under sperm competition Prediction: –relative testis size will be larger in species that roost in larger social groups (under the assumption that females in larger groups are more likely to mate multiple times)

23. 23 Variation in testis size and social group size among fruit bats and flying foxes (Fig. 9.11b)

24. 24 The comparative method and phylogeny The comparative method must take into account phylogenetic relationships among the taxa being studied This can be done using Felsenstein’s method of phylogenetically independent contrasts

25. 25 Pseudoreplication in comparative analyses (Fig. 9.12) If the common ancestor of taxa A-C had small testis size and small group size, then these three taxa represent only one evolutionary acquisition of small testis size and small group size. Likewise if the common ancestor of taxa D-F had large testis size and large group size

26. 26 Felsenstein’s method of evaluating comparative hypotheses using phylogenetically independent contrasts (Fig. 9.13)

27. 27 Phylogeny, group size, body mass, and testis mass in fruit bats and flying foxes (Fig. 9.14a)

28. 28 Correlated evolution of testis size and group size in fruit bats and flying foxes (Fig. 9.14b, c)

29. 29 Testis size and social group size in bats: Is it really sperm competition? What additional data would help to test the hypothesis that sperm competition drives the observed positive relationship between social group size and relative testis size? Can you think of an alternative explanation (besides sperm competition)?

30. 30 Phenotypic plasticity as an adaptive strategy Phototaxis in Daphnia magna (De Meester, 1996) – 1 Phenotypic plasticity means that the same genotype may express different phenotypes In general, quantitative phenotypes are plastic However, the term phenotypic plasticity is generally reserved for situations where the plasticity increases fitness (i.e., is adaptive) Daphnia magna is a small fresh-water crustacean Reproduces parthenogenetically Clones vary in their response to light (phototaxis) Phototactic behavior may be plastic within clones Daphnia from lakes that have fish (visual predators) tend to be more negatively phototactic when they sense fish

31. 31 Pictures of Daphnia

32. 32 Variation in phototactic behavior of Daphnia from three Belgian lakes (Fig. 9.17) Blankaart has many fish; Driehoekvijver has few fish; Citadelpark has no fish

33. 33 Phenotypic plasticity as an adaptive strategy Phototaxis in Daphnia magna (De Meester, 1996) – 2 Most clones from the lake with fish have a plastic phototactic behavior Most clones from lakes with few or no fish are not plastic Therefore, phenotypic plasticity (for phototaxis) is itself a trait that can evolve (there is genetic variation for plasticity within and among lakes) A reasonable hypothesis is that the plasticity of phototaxis in clones from the lake with fish is an adaptation to reduce predation by fish How do you feel about the level of replication in this experiment? Can you design a stronger test of the hypothesis that plastic phototaxis is an adaptation to fish predation?

34. 34 Limits to adaptation Trade-offs Constraints Lack of necessary genetic variation

35. 35 Selection on female flower size in Begonia involucrata: A trade off – 1 Sexes in separate flowers (monoecious). Male and female flowers similar in size and appearance Bees tend to avoid female flowers (which don’t give a reward) in favor of male flowers But female flowers need bee visits (and pollen) in order to set seed. Therefore, bees are a strong selective force on female flower function What is the nature of selection imposed by bees on female flower size? –Stabilizing selection — best strategy is to look like an average male flower –Directional selection — if larger male flowers offer larger rewards then larger female flowers should be preferred by bees

36. 36 Selection on female flower size in Begonia involucrata (Fig. 9.19) (Agren and Schemske 1991)

37. 37 Flowers of Begonia involucrata Fig. 9.18a. Male flower (left) and female flower An inflorescence

38. 38 Selection on female flower size in Begonia involucrata: A trade off – 2 Bees strongly prefer to visit larger flowers This is directional selection for larger flowers (male as well as female) What keeps flower size from increasing? There is a trade-off between between flower size and number of flowers per inflorescence This suggests that there is net stabilizing selection on flower size What is the optimum balance between flower size and flower number? How does the plant maximize total seed set? Indeed, does a plant appear to maximize total seed set?

39. 39 Flower color change in Fuchsia excorticata: a constraint – 1 A bird-pollinated tree Flowers are green (5.5 days), then turn red over a period of 1.5 days, then remain on tree as red (5 days) (= 11 days total) Nectar is present during days 1 – 7 90% of pollen exported by day 7 Why do flowers turn red? –Cue to pollinators, which increases pollination efficiency Why bother to turn red, why don’t the flowers just drop off after 7 days?

40. 40 Flower color change in Fuchsia excorticata (Fig. 9.20)

41. 41 Flower color change in Fuchsia excorticata: a constraint – 2 The constraint that appears to prevent dropping of flowers before they turn red is the time required for pollen tube growth from the stigma to the ovary. Table 9.3 Pollen tube growth in Fuchsia excorticata (after Delph and Lively 1989) Days since pollination1234 Percentage of 10 flowers with pollen tubes in ovary 020%100%

42. 42 Host shifts in an herbivorous beetle: constrained by lack of genetic variation? (Futuyma et al. 1995) – 1 Herbivorous leaf beetle in genus Ophraella Each species feeds on one or several closely related species of composites (sunflower family, Asteraceae) For beetles, the ability to live on a particular host plant represents a complex adaptation that includes the ability to recognize a plant as a suitable host and the ability to deal with plant’s chemical defenses What determines the pattern of host plant use by beetles? Why do closely related beetles not use the same host plant?

43. 43 Phylogeny and host plant relationships of the leaf beetles, genus Ophraella (Fig. 9.21)

44. 44 Host shifts in an herbivorous beetle: constrained by lack of genetic variation? (Futuyma et al. 1995) – 2 Hypothesis 1: all host shift are genetically possible. The actual distribution of beetles over host plants is due to ecological or chance factors Hypothesis 2: Most host shifts are genetically impossible. Most beetle species lack sufficient genetic variation in their feeding preferences and detoxifying mechanisms to be willing to feed on and/or to survive on alternate host plants

45. 45 Host shifts in an herbivorous beetle: constrained by lack of genetic variation? (Futuyma et al. 1995) – 3 Estimated genetic variation in beetles for feeding on or surviving on novel hosts using 4 beetle species and 6 host plant species (no genetic variation = no potential for adaptation to new host) –no evidence of genetic variation in 18 of 39 tests of whether adults or larvae would recognize and feed on a potential host –no evidence of genetic variation for larval survival on potential hosts in 14 of 16 tests These results suggest strong genetic constraints on host-plant shifts If hypothesis 2 is correct, we can also predict that beetles will be more likely to show genetic variation for host plant feeding and survival when potential hosts are closely related to the beetle’s actual host, or are hosts of closely related beetles (see Table 9.4) –Genetic variation for feeding in 7/8 tests when novel plant is in same tribe as beetle’s actual host, but only 14/31 when plant is in different tribe –Genetic variation for feeding in 12/16 tests when novel plant is host to a beetle in same major clade as tested beetle, but only 9/23 tests when plant is host to a beetle in a different major clade

46. 46 Selection operates on different levels In our example of HIV, we noted that at the level of virions within individual hosts, selection favored virions that could evade the host immune system, as well as develop resistance to drugs – in other words, virions that end up killing the host individual At the level of virions in the entire host population, however, the best long-term virion strategy might be to reduce host mortality – because causing exinction of the host population would be a bad strategy for HIV Would it be possible for natural selection on HIV to favor reduced host mortality?

47. 47 Selection operates on different levels: mitochondria in yeast - 1 Non-respiratory (parasitic) mitochondria replicate faster than normal mitochondria that carry out aerobic respiration Yeast cells with normal mitochondria replicate faster than yeast with non-respiratory mitochondria Selection on mitochondria operates on two levels: –The level of the population of mitochondria within an individual yeast cell – where non-respiratory mitochondria “win” because they replicate faster –The level of yeast cells within a culture – where normal mitochondria may “win” because the yeast cells that contain them replicate faster Which level wins depends upon the relative strengths of selection

48. 48 Selection operates on different levels: mitochondria in yeast - 2 Experimental system (Taylor et al. 2002) Start populations of yeast that contain a mixture of normal and parasitic mitochondria in each cell Grow yeast at small, medium, and large population size Small population size = weak selection at the level of yeast cells within culture: favors parasitic mitochondria Large population size = strong selection at the level of yeast cells within culture: favors normal mitochondria because they increase the fitness of the yeast cells that carry them Determine the proportion of cells that had only parasitic mitochondria after 150 generations.

49. 49 Selection on cells in populations versus selection on mitochondria in cells (Fig. 9.22)

50. 50 Selection operates on different levels: mitochondria in yeast - 3 Note: an important difference between these HIV and mitochondria examples is that mitochondria are transmitted vertically only. (HIV is most commonly transmitted horizontally.) This means that the fitness of the host cell or individual is crucial to the fitness of mitochondria (at least when selection is acting on the host), but not to the fitness of HIV

51. 51 Analysis of adaptation: Summary Hypotheses about the adaptive value of a trait should be tested –Experimental manipulation, observation, comparative method There are limits to adaptation –Trade-offs (pleiotropy), constraints, lack of genetic variation A complete understanding of the adaptive value of a trait may require analysis of selection on more than one level