Natural Selection Survival Mating Success Parental Care Intrasexual Mate Choice Competition (Epiga

1. Natural Selection Survival Mating Success Parental Care Intrasexual Mate Choice Competition (Epigamic) Sexual Selection

2. Sexual Selection

3. Intrasexual Selection Epigamic Selection

4. Intrasexual or Epigamic Selection? Or both?

5. Epigamic Selection has received most of the theoretical attention. Q: What exactly do females see in these guys (besides a pretty face)? History of theories about epigamic traits and female choice.

6. Adaptive Choice Non-adaptive Choice Fisher (1930) – male trait initially correlated with fitness Trivers (1972) – female choice and parental investment key Zahavi (1975) – good genes idea and handicap principle Hamilton & Zuk (1982), Kodrik-Brown & Brown (1984) – epigamic traits as honest signals of quality or condition Grafen (1990) – makes the handicap principle an honest woman Darwin (1859) – females have a ‘sense of beauty’ Fisher (1930) – runaway selection due to female preference Lande (1981), Kirkpatrick (1982) – covariance (Quixotic female) models: no correlated fitness advantage necessary Trivers (1985): “The field is now wide open and many opinions are possible. Indeed, it remains to be seen whether female choice is an arbitrary and amusing evolutionary sideshow or a powerful force driving male evolution for female benefit.”

7. Epigamic Selection: The Land of Many Theories (and for the most part these are not mutually exclusive) • Direct benefits – Female choice leads to increased fecundity (more offspring). • Good genes – Female prefers signals of male genetic quality that increase survival of their offspring. • Runaway selection – Female preference increases because it is linked to ‘sexy son’ advantage. • Handicap selection– Female prefers signals that are handicaps because they signal good genes. • Sensory exploitation – Male evolves display trait that exploits pre-existing sensory bias in female. • Chase-away selection – female preference then evolves away from male traits if there is a cost to being exploited.

9. Fisher: Runaway Selection “Fisher’s (1930) brief discussion of runaway sexual selection is notorious for both its insight and its impenetrability” (Ryan 1997).

10. Fisher: Runaway Selection Basic idea: female preference for a male trait (say tail length) will be favored because female with that preference will have ‘sexy’ successful sons (thus increasing her RS). Assumption: female preference has genetic basis (as does male trait).

11. Fisher: Runaway Selection “Runaway” refers to positive feedback between trait & preference. Genes for trait and preference will become associated. Female Preference Male Trait Positive Feedback Loop

12. Fisher: Runaway Selection Hard to test. Perhaps best approach: test the assumption of a correlation of male trait and female preference. Bakker (1993):sticklebacks Took males and females from stickleback populations where they varied in terms of brightness of male nuptial correlation (presumably related to intensity of predation). Crossed fish from bright population with fish from dull population. Sons intensity of red correlated with that of their fathers’. Daughters of red males preferred red over dull males, while daughters of dull males tended to show no preference. Wilkinson & Reillo (1994): stalk-eyed flies. Selection expts – selected for long eye span, for short eye span, unselected. After 13 generations, females from long eye span and unselected lines prefer long eye span males, females from short eye span prefer short eye span males.

13. 1972

14. Female Choice General sex differences: Male: ardent, indiscriminant Female: reluctant, discriminating ♀ ♀ Revived role of female (mate) choice in sexual selection

15. Trivers: key to sexual selection is parental investment (PI) • Initial PI (female's provisioning of egg cell) • Specialized PI (mammary glands, incubation patches, etc) – usually supplied by one sex only, almost always the female • female’s nourishing of the embryo • female’s producing yolk-filled egg (reptiles & birds) • incubation (reptiles and birds) • female lactation • Generalized PI – usually behavioral, supplied by either sex • guarding the offspring • feeding the offspring • defending territory/nest used for feeding & protecting young

16. SEXUAL SELECTION • Trivers: Key to sexual selection is parental investment (PI). • Trivers: Sexual selection = • Sex investing less will compete for sex investing more (intrasexual selection) • 2. Sex investing more will be discriminating in choosing mates (epigamic selection) • Typically: Female PI > Male PI • so usually its males competing among themselves for females and females choosing among males.

17. Trivers: Differential PI Drives Sexual Selection Female PI ? Sexual Selection ♂ - ♂ See recent theoretical papers by Hanna Kokko et al

18. Sex role reversals Seahorses & Pipefish – ♂ specialized PI Mormon crickets – ♂ spermatophores Jacanas – Polyandry, ♂ parental care In all* these cases, ♂♂ are the more choosey sex and/or females compete among themselves for males • Trivers: Sexual selection = • Sex investing less will compete for sex investing more (intrasexual selection) • Sex investing more will be discriminating in choosing mates (epigamic selection)

19. The Handicap Principle (Zahavi 1975) “An individual with a well developed sexually selected character [such as a peacock's flashy tail] is an individual which has survived a test. A female which could discriminate between a male possessing a sexually selected character, from one without it, can discriminate between a male which has passed a test and one which has not been tested. Females which selected males with the most developed characters can be sure that they have selected from among the best genotypes of the male population.”

20. The Handicap Principle (Zahavi 1975) Two Ideas: (1) female choice for good genes (2) ideal trait for that purpose = handicap

21. Wow, how attractive am I!! The Handicap Principle (Zahavi 1975) Good genes part was popular but the handicap principle seemed implausible to many. Theoreticians tried to see if it could be modeled – most attempts failed.

23. Lande 1981; Kirkpatrick 1982, 1986: The Handicap Mechanism Does Not Work. Kirkpatrick 1986 Alternative: Arbitrary Female Preferences

24. Some took up the good genes part of Zahavi’s idea (ignoring the handicap part). Hamilton, W.D. & Zuk, M. 1982. Heritable true fitness and bright birds: a role for parasites? Science 218: 384-387. Kodric-Brown, A. & Brown, J. H. 1984. Truth in advertising: the kinds of traits favored by sexual selection. American Naturalist 124: 309-323.

25. Hamilton & Zuk 1982 Bright Birds and Parasites Birds are susceptible to parasites, both external and internal. Natural selection should favor female choice for parasite-resistant males. How to choose? Parasitized birds have dull plumage. Therefore, natural selection should favor female choice for males with brighter-than-average plumage.

26. Hamilton & Zuk 1982 Bright Birds and Parasites Butwhydo malesevolvetobesoextremelybright? Because parasites evolve ways to defeat resistance. Once a new parasite form arises, natural selection again favors males who can resist the parasite. In other words, natural selection favors females who choose males with still brighter plumage. Thus, coevolution between host and parasite leads to brighter and brighter males.

27. Here come the empirical studies! • (especially manipulations studies) • Do females prefer males with exaggerated traits? • Are males with exaggerated traits higher-quality males? • Do males with exaggerated traits have (more) good genes? Long-tailed widowbird

28. Mean no. of nests per male Andersson, M. (1982) Female choice selects for extreme tail length in a widowbird. Nature 299: 818-820.

29. Andersson, M. (1982) Female choice selects for extreme tail length in a widowbird. Nature 299: 818-820.

30. Barn Swallow tail-lengthening experiments (Moller 1988)

31. Pryke, S. R. & Andersson, S. 2002. A generalized female bias for long tails in a short-tailed widowbird. Proc. B 269: 2141-2146.

32. Petrie et al 1991 Males with more eye spots mate with more females. Females choose males with more eyespots ... but is it because they have more eyespots?

33. Petrie & Halliday 1994 controls -20 eyespots Cut out eyespots on some males and did mate choice tests. Females prefer males with more eyespots ... but are they better quality males?

34. Loyau et al 2005 Meaured heterophil count (these are white blood cells that go up when animal is fighting infection). Males with more eyespots are healthier … but is this fitness different heritable?

35. Petrie 1992 % of chicks surviving after 2 years Apparently they are better quality males (pass on better genes) Meanareafather’seyespots(mm2) 8 males X 4 females each 96 offspring released

36. cost low quality benefit Fitness cost or benefit optimum cost high quality Signal intensity An epigamic signal will be an honest indicator of condition or quality of male if its less costly (smaller handicap) for good condition (hi quality) male than for lo condition (lo quality) male

37. cost low quality benefit Fitness cost or benefit optimum cost high quality Signal intensity Indicator trait (ornament or display) is a handicap in that it is costly or difficult to produce, and is supported by many genes affecting overall fitness, such as genes for disease resistance.

38. Sensory Exploitation hypothesis: Male evolves display trait that exploits pre-existing sensory bias in female. Makes unique prediction that in phylogeny, female bias (preference) existed before male trait evolved (vs. evolved together, or male trait evolved before female preference) = correlated evolution hypothesis

39. Sensory Exploitation Physalaemus pustulosus adds ‘chuck’ to end of its advertisement calls (whine-chuck). P. coloradorum males make just the whine. Experiments show that females of both species prefer a call with a chuck.

40. Sensory Exploitation

42. Grafen on Handicaps & Signalling (aka: Grafen makes Handicap Principle an Honest Woman) • Handicaps suggested by Zahavi (1975) • Handicaps contested • A model of the handicap principle • Lessons from the model

43. Basic Ideas of Female Choice Models • Males must vary in a way that matters to females (call it ‘quality’), but is invisible to them • Males must express an observable trait, which can depend on ‘quality’. • The male strategy is a function that says how the observable trait depends on quality • 3. Females can draw an inference about the invisible trait from the observed trait. • The female strategy is a function that says how the inferred quality depends on the observed trait.

44. Basic assumptions of Handicap Model, Grafen version 1. The tail is costly i.e. a longer tail leads to lower fitness (all other things held equal) 2. A female’s fitness is higher, the more accurately she assesses the quality of males 3. A male is fitter the more highly his quality is assessed by females. Differential cost assumption: 4. The ratio of the marginal cost of advertising to the marginal advantage of improved assessment must be an increasing function of quality

45. tail quality quality tail A male who has a short tail whatever his quality A female who views all males as average quality A male who has a longer tail if he turns out of higher quality A female who interprets a longer tail to mean higher quality A male who has a shorter tail if he turns out of higher quality A female who interprets a shorter tail to mean higher quality A male who has a long tail whatever his quality A female who views all males as high quality Can we find a male strategy and a female strategy such that, if the population is all playing those strategies, an individual couldn’t increase his or her fitness by choosing a different strategy?

46. tail quality quality tail A high quality male could gain by breaking the rule and having a shorter tail -- the tail would cost less and females would rate him just the same. Therefore this is no equilibrium. Can we find a male strategy and a female strategy such that, if the population is all playing those strategies, an individual couldn’t increase his or her fitness by choosing a different strategy?

47. tail quality quality tail Females are correctly inferring quality from tail length – so they are optimal. Provided longer tails are costlier for lower quality males, then neither low nor high quality males can gain by changing. Therefore this is an equilibrium – the ‘signalling equilibrium’. Can we find a male strategy and a female strategy such that, if the population is all playing those strategies, an individual couldn’t increase his or her fitness by choosing a different strategy?

48. What does the model do ‘locally’? • Shows Zahavi’s idea works • Makes assumptions explicit • Constructs a useful logical framework (strategy is a function) • Identifies the handicap model as about signalling, and shows how to make progress with signalling ideas

50. Female preference + +