Finicky Females and Macho Males: Sexual Selection in Two Arthropods

1. Finicky Females and Macho Males:Sexual Selection in Two Arthropods • Vik Iyengar • Department of Biology • Villanova University

2. Sexual Selection • Fundamental question that troubled Darwin • Why do some males have such gaudy traits that would appear to decrease survival? • Sexual selection • Differential reproductive success due to competition over access to mates 1. Intrasexual selection • Members of one sex compete for access to the other sex • Usually male-male competition 2. Intersexual selection • Members of one sex choose the other • Usually female choice

3. Intrasexual Selection and “Armaments” • “King of the Hill” (usually male-male competition) • No opportunity for active female choice if only 1 guy left … but large variance in male RS • Examples? • Elephant seals, red deer (elk), giraffes, stalk-eyed flies

4. Acorn barnacle (Semibalanus balanoides) IntrasexualConflict Gone Wild! • Lucky Ducks?! • Argentine lake duck (Oxyuravittata) • Penis is 32.5 cm coiled, up to 42.5 cm! • Barnacle Shenanigans! • Crazy fact: Barnacles have the largest penis to body size ratio in the Animal Kingdom! 10 x

5. Intersexual Selection and “Ornaments” • Members of one sex choose certain mate of other sex • Usually female choice (select males worthy of investment) • Examples • Visual = quetzals, bowerbirds • Acoustic = crickets, frogs • Chemical = moths and butterflies

6. Why do females choose certain males? • Two Categories of Benefits (1) Direct benefits = non-genetic resources from mate • Increase in female survival • Increase in female fecundity • Increase in offspring survival • Examples • Male birds that incubate or provide food • Giant water bugs rent egg space • Australian redback spider and sexual cannibalism

7. Why do females choose certain males? • Two Categories of Benefits (1) Direct benefits = non-genetic resources from mate (2) Indirect benefits= genes from mate • “Sexysons” (Fisher 1930) • Sons inherit that genes that made the father so attractive • “Goodgenes” (Zahavi 1975) • Offspring of preferred males have higher fitness because females are basing choice on honest indicators of quality • Selection for characters correlated with foraging ability, etc. * Not mutually exclusive *

8. Utetheisaornatrix The Rattlebox Moth Megalorchestiacaliforniana The California Beach Flea Signs of sexual selection: dimorphic sexes ♀ ♀ ♂ ♂

9. Megalorchestia californiana (The California Beach Flea) • Extreme sexual dimorphism! • Male characteristics • Large, orange-red antennae • Enlarged 2nd pair of gnathopods • Female characteristics • Mate once per year • Eggs available for fertilization • for only a few hours after molting • Eggs and juveniles retained • in a brood pouch ♀ ♂ gnathopod peduncle flagellum

10. Beach combing with amphipods • Habitat & Food Preferences • Native to sandy beaches along the coast in the Pacific Northwest • Found in burrows under beach wrack (prefer bull kelp) • Feed on dead and decaying material • Other characteristics • Most active at dusk and dawn • Walk upright; can move/hop fast! • Harem mating system?

11. Overarching Question Given the sexual dimorphism, including bright coloration and weaponry in males, is female choice or male-male competition more important in shaping the mating system? ♀ ♂ gnathopod peduncle flagellum

12. Q1: Are male characters correlated? • Methods • Measure length of thorax, antennae • Color of antennae measured using photographs with color standard • Results • Male body mass was positively correlated with both male body length (r2=0.816, F1,148=658.54, P<0.001) and total antennal length (r2=0.846, F1,148=810.08, P<0.001) • Negatively correlated with peduncle hue (r2=0.327, F1,22=10.67, P<0.005). • Conclusion • Both males and females can assess male quality based on antennal color 30 25 20 Peduncle hue 15 10 5 0 150 200 250 300 350 400 450 500 Male body mass (mg)

13. Q2: Which is more important, female choice or male competition? • Methods • Place 3 amphipods (2M:1F) in container with two burrow locations • Movement of some individuals restricted by wire mesh • Results • Conclusion • Male • competition • rules!

14. Q3: What are dispersion patterns in a more natural setting? • Methods • Large sand arena with 9 sections • Single sex: 9 Males or 18 Females • Mixed sex: 9 Males and 18 Females • Results • Single sex (9M): Males distributed different than random (X2=31.30, df=4, P<0.001) and consistent with a uniform distribution (Id=56.10, df=89, P>0.975). • Single sex (18F): Females were randomly distributed (X2=5.92, df=6, P=0.43). • Mixed sex (9M+18F): both sexes had a clumped distribution different from their same-sex distribution (Males: X2=107.61, df=5, P<0.0001; Females: X2=120.72, df=6, P<0.0001). Males with females were larger than those found alone (t=2.46, df=88, P<0.05) 54 350 36 300 250 Body Mass (mg) 200 150 100 50 0 Males Males Alone with Females

15. Megalorchestia californiana (The California Beach Flea) • Remaining Questions • Behavior in the field? • Effects of fighting success and burrow occupancy on reproductive success? • Environmental effects (e.g., sex ratio, • food abundance) on repro success? ♀ ♂ gnathopod peduncle flagellum

16. Utetheisa ornatrix The rattlebox moth

17. Utetheisaornatrix: The Early Years Is the moth chemically protected? Ask a spider…

18. Better living through chemistry! With PA…and Without Pyrrolizidine Alkaloid = PA

19. All life stages are protected by PAs

20. Finding a mate ♂ ♀

21. Male courtship: Wave your pom-poms! Coremata contain a male-specific, short-range courtship pheromone

22. Male pheromone (HD) is derived from PA Females choose males based on HD

23. Why choose males based on pheromone levels? Pheromone levels correlated with: • ALKALOID LEVELS • BODY SIZE (Size matters!) • SPERMATOPHORE SIZE SEXUAL SIZE DIMORPHISM Males larger than females Spermatophore (≈10% body mass): (1) Alkaloid- protect female & eggs (2) Nutrient- major component, used to increase fecundity (3) Sperm- females use sperm from larger males

24. Why do Utetheisa females choose big males? • Sexual Selection in Utetheisa • DIRECT SELECTION= non-genetic resources from mate • Increase in female survival • Increase in female fecundity • Increase in offspring survival • INDIRECT SELECTION= genes from mate • “Sexy Sons” (Fisher 1930) • Sons of preferred males have higher mating success • “Good Genes” Benefits (Zahavi 1975) • Offspring of preferred males have higher fitness because females are basing choice on honest indicators of quality YES!!! YES!!! YES!!! ?

25. Heritability of body size Question: Do larger individuals have larger offspring? Answer: YES, for all parent-offspring combinations! (autosomal inheritance) …but which genetic benefits do choosy females reap? [Iyengar, Reeve & Eisner 2002]

26. General Methods Non-preferred male (Same-size sisters) EGGS EGGS n ≈ 40 offspring of non-preferred males n ≈ 40 offspring of preferred males

27. Fecundity of Daughters Non-preferred Daughters Preferred Daughters (Same-size) (Brothers) (Same-size) (Brothers) (Same-size) (Brothers)

28. Paired t-test p < 0.05 450 400 350 300 Mean Fecundity (number of eggs laid) 250 200 150 100 50 Preferred Non-preferred 0 RANDOM DAUGHTERS Fecundity of Daughters Corresponds to 8% difference ≈ 30 eggs

29. Mating Success of Sons Non-preferred Sons Preferred Sons (random females)

30. Mating Success of Sons Randomly-selected sons of preferred males have higher mating success. 22/30 were more successful in courtship (sign test, p < 0.05)

31. Why do Utetheisa females choose big males? • Sexual Selection in Utetheisa • DIRECT SELECTION= non-genetic resources from mate • Increase in female survival • Increase in female fecundity • Increase in offspring survival • INDIRECT SELECTION= genes from mate • “Sexy Sons” (Fisher 1930) • Sons of preferred males have higher mating success • “Good Genes” Benefits (Zahavi 1975) • Offspring of preferred males have higher fitness because females are basing choice on honest indicators of quality YES!!! YES!!! YES!!! YES!!! YES!!!

32. Testing Assumptions of Sexual Selection • Genetic assumptions for indirect selection: • 1) Trait under selection must be heritable • 2) Mating preference for the trait must be heritable • 3) The trait and mating preference must be correlated P

33. Mating Preference Index Calculation 10% difference 5% difference 10% difference 5% difference 10% difference 5% difference Focal Female MPI values ranged from 0 to 1 (average score of the six trials)

34. Heritability of Mating Preferences • • Three generations of 44 families • * 1st generation: Paternal grandmother (inheritance via father) • * 2nd generation: Mother • * 3rd generation: Average of 6 full sisters • (Grand)parent-offspring regression of MPI values Heritability calculated based on regression slope and relatedness

35. Mean mating preference index (MPI) of females plotted as a function of the MPI of their mother and paternal grandmother .7 .7 .6 .6 Mean MPI of Females Mean MPI of Females .5 .5 .4 .4 .3 .3 0 0.2 0.4 0.6 0.8 1.0 0 0.2 0.4 0.6 0.8 1.0 MPI of Mothers MPI of Paternal Grandmothers r2 = 0.025, n = 44, P = 0.305 h2 = -0.108 ± 0.10, P = 0.303 r2 = 0.333, n = 44, P < 0.0001 h2 = 0.513 ± 0.112, P < 0.001

36. ZZ/ZW sex chromosome systems • All lepidopterans and birds • Males homogametic (ZZ) • Females heterogametic (ZW) Genetic architecture and heritability in Utetheisa • Z-linked mating preferences • No autosomal variation

37. Transmission of Z-linked mating preferences ZW ZZ ZW ZZ ZW ZW ZZ ZZ

38. Testing Assumptions of Sexual Selection • Genetic assumptions for indirect selection: • 1) Trait under selection must be heritable • 2) Mating preference for the trait must be heritable • 3) The trait and mating preference must be correlated P P

39. Correlation between mean mating preference index (MPI) of females and the body mass of their fathers in Utetheisa ornatrix .7 Larger males have daughters with stronger preferences for large males .6 Mean MPI of Females .5 .4 .3 60 80 100 120 140 Father Body Mass (mg) r2 = 0.232, n = 44, P < 0.001

40. Testing Assumptions of Sexual Selection • Genetic assumptions for indirect selection: • 1) Trait under selection must be heritable • 2) Mating preference for the trait must be heritable • 3) The trait and mating preference must be correlated P P P

41. Implications of Heritability Results • • The female mating preference is sex-linked • - Fathers are ZZ, and pass on Z-linked traits • to their daughters. * Inheritance analogous to male baldness in humans! • Non-random tendency for gene(s) to occur on Z - Arctiid moths average 31 pairs of chromosomes - Sex chromosomes not unusually large - Probability of mating preference gene(s) occurring on Z: 1 gene: (1/62) = 0.016 2 genes: (1/62) (1/62) = 0.00026

42. Protected Invasion Theory • • Genes will be especially protected from random loss due to genetic drift if there are multiple copies * In ZZ/ZW genetic systems, (1) Genes on Z especially protected (2) When preferences are Z-linked, more sons will have the preferred trait and carry the preference than in other genetic systems These sons will have enhanced mating success

43. Protected Invasion Theory Female Mating Preference Preferred Male Trait AutosomalX-linkedZ-linked AA AA ZW ZZ XX XY XY XY ZZ ZZ AA AA AA AA  ½ sons  ¼ sons No sons

44. Summary of Protected Invasion data • The female mating preference is strictly • paternally inherited. • • Female mating preferences resemble • those of their paternal grandmother. • Due to the genetic architecture, • mating preferences are Z-linked. • • Inheritance via father (and not mother) means that • the preference gene(s) in Utetheisa lie mostly • or exclusively on the Z chromosome.

45. Summary of Protected Invasion data • Non-random tendency for female preference genes to occur on Z • Genetic architecture may play a role in sexual selection • Protected Invasion Theory predicts exaggerated male traits are more likely to occur when traits are Z-linked - Explanation of widespread occurrence in lepidopterans and birds?

46. Utetheisaornatrix The Rattlebox Moth Megalorchestiacaliforniana The California Beach Flea Acknowledgments Collaborators Tom Eisner Kern Reeve Alex Bezzerides Carmen Rossini Collaborators Bianca Starks Nydia Brooks Joshua Graber Funding Sources State University of New York Fellowship NSF Predoctoral Fellowship Sigma Xi Grant-in-Aid of Research Funding Sources Friday Harbor Laboratories Makah Tribal Council (Clallum Co., WA) (Thanks)

48. Precopulatory Battles: Armaments are common • Tradeoffs • More weaponry means less energy for sperm production …but usually more than compensated by higher mating success! From Emlen (2008)

49. Heritability Methods Wild Female 1 Wild Female 2 Eggs Eggs 7-9 larvae 7-9 larvae EGGS 7-9 larvae 7-9 larvae 7-9 larvae 7-9 larvae 7-9 pupae 7-9 pupae 7-9 pupae 7-9 pupae

50. Body size is heritable! 280 r2 = 0.426, p < 0.01 260 Do females, by mating with larger males, have offspring with higher fitness? (1) Fecundity of Daughters (2) Mating Success of Sons Sons 240 Daughters 220 r2 = 0.210, p < 0.01 200 180 160 140 N = 60 families 100 120 140 160 180 200 220 240 260 280 300 MEAN OFFSPRING PUPAL MASS (mg) FATHER PUPAL MASS (mg) 280 r2 = 0.181, p < 0.01 260 Sons 240 Daughters 220 r2 = 0.222, p < 0.01 200 180 160 140 100 120 140 160 180 200 220 240 260 280 300 MOTHER PUPAL MASS (mg)