Evolution of extra-pair copulation -------- Sexual selection and mating systems

1. Evolution of extra-pair copulation -------- Sexual selection and mating systems Dominique Allainé UMR-CNRS 5558 « Biométrie et Biologie Evolutive » Université Lyon 1 France allaine@biomserv.univ-lyon1.fr

2. Sexual selection Why do the sexes differ so much ?

3. Sexual selection An answer to this question has been proposed by Charles Darwin in his book of 1871 ‘The descent of man, and selection in relation to sex’: The sexual selection Definition Sexual selection is that selection which occurs within one sex as a result of competition among members of that sex, for reproduction with members of the other sex C.R. Darwin Sexual selection is a special process that shapes the anatomical, physiological, and behavioral mechanisms that function shortly before or at the time of mating and serve in the process of obtaining mates E.O. Wilson

4. Sexual selection Darwin tried to explain the evolution of secondary sexual characters by the battle between males to charm females and by the female preference for certain male traits. • So, he recognized two components of the sexual selection: • Male-male competition • Female mate choice

5. Big ovule  Slow rhythm of ovulation  Limited number of offspring  Maternity certainty Maximize their quality    High maternal investment Adequate male      Access to resources Mate choice Female choice Sexual selection Reproductive strategy ♀

6. Small spermatozoids  fast rhythm of production  number of offspring unlimited  Paternity uncertainty Maximize their quantity    low paternal investment No mate choice Access to females   Male competition Sexual selection Reproductive strategy ♂

7. Sexual selection Female choice: definition The mate choice is defined as any pattern of behavior shown by members of one sex that leads to their being more likely to mate with certain members of the opposite sex than with others. Halliday 1983 Females are expected to be selective on the quality of their partners and this is not the case for males. So, mate choice generally refers to female choice If a consensus exists among females for the preferred traits, then female choice may be a selection pressure in favor of preferred traits and this may lead to the evolution of secondary sexual traits in males

8. Sexual selection Female choice: mechanism Cues used by females • morphological

9. Sexual selection Female choice: mechanism Cues used by females • behavioral Willow warbler

10. Sexual selection Female choice: evolution Why females should prefer such traits ? In particular, females often show a preference for traits that should not be favored by natural selection. For example, long tails, big antlers bright and colored plumages should not be advantageous for the survival of males. Darwin had no explanation of why female preferences for traits that hinder rather than help male survival should have evolved.

11. Sexual selection Female choice: evolution • Fisher’s runaway process Preference for arbitrary traits that are not necessarily adaptive (example: antlers’ size, tail length …) but the attractiveness is genetically determined. To explain why the preference spreads in the population, he assumed, at the initial stage of the process, that the preferred trait correlated with a selective advantage (survival enhancement) of the male possessing the trait. If most females prefer males having the exaggerated trait, any female that did not show this preference would have fewer descendants because her sons would get fewer mates. When the process is under the way, females do not choose males because he is better than males not possessing the trait but because their sons will be more attractive to females.

12. Sexual selection Female choice: evolution • Fisher’s runaway process When the process is under the way, there is also a continuing and accelerated increase both in male trait and in degree of preference. Fisher called this the runaway process. If carried far enough, it is evident that sufficiently severe counter selection in favor of less ornamented males will be encountered to balance the advantage of sexual preference and the runaway process will end.

13. Sexual selection Female choice: evolution • Choice for direct benefits Females may prefer male traits that signal the ability of males to increase their reproductive success : • choice for fertility insurance • choice for paternal care • choice for a male in good phenotypic condition

14. Sexual selection Female choice: evolution • Choice for direct benefits • choice for immediate benefits

15. Sexual selection Female choice: evolution • Choice for indirect benefits Females may prefer male traits that signal the ability to produce offspring of high genetic quality : • choice for ‘good genes’ • viability • resistance to parasites • choice for ‘compatible genes’ • genetically dissimilar • avoidance of intragenomic conflicts Preferred traits may be costly in fitness term (handicap principle) Preferred traits cannot be imitated (honest signal)

16. Sexual selection Female choice: evolution • Choice for indirect benefits The choice for good genes implies that females prefer a unique best male. Genetic effects are additive and male display signals possession of good genes But this raises the problem of the persistence of additive genetic variance in fitness

17. Sexual selection Female choice: evolution • Choice for indirect benefits The choice for compatible genes implies that females do not prefer a unique best male. Genetic effects are not additive. This solves for the problem of maintaining additive genetic variance But this raises the problem of the evaluation of the mate’s genetic make-up

18. Sexual selection Male competition • Before copulation • Direct fights Males may compete directly by fighting. In general, the strongest males win the competition and have access to females.

19. Sexual selection Male competition • Before copulation • Visual display: nuptial parade Males may compete by exhibiting the more attractive parade to charm females. In general, males showing the longest or the more colored parade win the competition.

20. Sexual selection Male competition • Before copulation • Acoustic display Males may compete by exhibiting the more attractive song to charm females. In general, males having the longest or the more complex song win the competition.

21. Sexual selection Male competition • After copulation and before fertilization Sperm competition (Parker 1970) ➨ The sperm of more than one male compete … … to fertilize the eggs of the female. Females may leave the competition open to maximize the chance that the best sperm fertilizes their eggs Females may choose the sperm that fertilizes their eggs (cryptic female choice)

22. Sexual selection Male competition • After copulation and before fertilization Mechanisms reducing the opportunity for sperm competition • mate guarding (mammals, birds) • prolonged copulation (some primates) • frequent copulation (last male precedence, birds and insects) • vaginal plug (insects)

23. Sexual selection Male competition • After fertilization Bruce effect Infanticide

24. Sexual selection The opportunity for sexual selection is (Wade 1979): Imates = Vmates /x2mates So, the potential for sexual selection depends on the variance in the number of mates per males and then should differs according to the different mating systems as previously thought by Darwin

25. ♀ ♀♀ ♂ ♂ ♀ ♀ ♂ ♂ ♀ Mating system Sexual selection is assumed to be: • strong in polygynous species High variance of reproductive success in males • stong in promiscuous species High variance of reproductive success in males ♂ ♂♀ ♂ • strong in polyandrous species High variance of reproductive success in females

26. ♂ ♀ • weak in monogamous species Mating system Sexual selection is assumed to be: Low variance of reproductive success in males No sexual dimorphism

27. Mating system The myth of monogamy ‘‘ Well over nine-tenth (93%) of all passerine subfamilies are normally monogamous…’’ Lack (1968) But

28. Mating system The myth of monogamy How to explain sexual dimorphism in monogamous species ? Monogamy: an ambiguous concept Monogamy refers to a social mating system = social monogamy social monogamy ➨ formation of pair bonding Monogamy refers to a genetic mating system = genetic monogamy genetic monogamy ➨ copulation with an exclusive partner

29. Mating system The myth of monogamy Until recently, the evolution of monogamy was explained by the constraints enforcing pair living and social monogamy was largely assimilated to genetic monogamy But Behavioral observations reveal occurrence of extra-pair copulation (EPC) If EPC leads to extra-pair paternity (EPP) and if EPP is important, then our perception of sexual selection in monogamous species may be modified Molecular data give evidence of occurrence of extra-pair paternity

30. Mating system The myth of monogamy Extra-pair paternity is almost the rule in birds Extra-pair paternity occurs in 75% of socially monogamous bird species Extra-pair paternity is common also in mammals

31. Mating system The myth of monogamy social monogamy genetic monogamy ➨ Socially monogamousbut Mixed strategy = pair bonding + extra-pair copulation • If some males are very successful in gaining extra-pair paternity • - either because of a greater ability or because they are preferred • as extra-pair mates - at the expense of other males, then : • the variance of reproductive success in males may be greater than • thought • traits of successful males should spread in the population This could explain sexual dimorphism observed in some socially monogamous species

32. Mating system The myth of monogamy Møller et Birkhead (1994)  analyse des causes évolutives des copulations hors couples

33. Males Females  Number of partners Number of partners Mating system The evolution of EPC Benefits of extra-pair copulation ??? Active participationof both males and females ? Offspring number

34. Mating system The evolution of EPC Benefits to females 1 EPC is viewed as a mean for females to modify their mate choice Females may seek EPC to gain direct benefits • Fertility insurance hypothesis • EPC: chance to mate with a fertile male • Parental care hypothesis • EPC: amount of paternal care • Infanticide hypothesis • EPC: uncertainty on paternity and the risk of infanticide

35. Mating system The evolution of EPC Benefits to females 2 Females may seek EPC to gain indirect benefits • Good genes hypothesis • EPP: possession of good genes in offspring • many supports: birds • Genetic compatibility hypothesis • EPP: genetic compatibility of offspring’s genome • supports are going increasingly: birds • Genetic diversity hypothesis • EPP: genetic diversity among young within the litter • few support : insects

36. Genetic diversity systematic EPM = WPM EPY=WPY • when genetic compatibility  Genetic compatibility Compatibility: EPM > WPM EPY>WPY  with possession of bad genes in social partner Good genes: EPM > WPM Good genes EPY>WPY Mating system The evolution of EPC Predictions hypotheses Social partner EPM vs WPM Offspring EPY vs WPY EPP occurrence characteristics performances

37. Mating system Alpine marmots Objective: Test of these predictions in the alpine marmotMarmota marmota

38. Mating system Alpine marmots Social structure Dominants ♀ ♂ Subordinates • Family(2 – 15) • Socially Monogamous • Reproductive suppression • One litter per year (4; 1-7) • Dispersal at 2 years (or later) ♀♀ ♂♂ Immatures Juveniles ♀♂ ♀♂

39. Mating system Alpine marmots Life cycle 3 years subordinate dispersal 3 years dominant dispersal 4 years and + subordinate 4 years and + dominant 2 years sexual maturity Reproduction Reproduction 1 year juveniles

40. ♀ ♂ ♂ ♂ ♂ ♂ related subordinate transient unrelated subordinate Mating system Alpine marmots Dominant ♀ ♂ m a t e c h o i c e ♂ ♂ ♀ other family ♂ ♂ ♂ male competition

41. female choice ➨ choice among available extra-pair males • competition between males ➨ availability of extra-pair males Mating system Alpine marmots Extra-pair copulation may result from both components of sexual selection

42. Mating system Alpine marmots Study site Natural reserve in the French Alps Alpine meadow at 2340 m asl

43. Mating system Alpine marmots Since 1990, 20 families are studied and 1016 individuals were marked For each family: number, age, sex and socialstatus of known individuals

44. DNA Amplification PCR DNA extraction Migration and analysis Mating system Alpine marmots Typing individuals for microsatellites tissue

45. Mating system Alpine marmots Typing individuals for microsatellites Heterozygous Homozygous

46. Mating system Alpine marmots Paternity analysis Data: individuals typed at 16 microsatelliteloci Incompatibility = 0 WPY Comparaison dominant female/ offspring Comparaison dominant male/ offspring Incompatibility >= 1 EPY

47. Mating system Alpine marmots • Genetic characteristics • Heterozygosity: individual standardized heterozygosity (Coltman et al. 1999) • Genetic similarity: Queller and Goodnight’s estimator • (Queller & Goodnight 1989) Composition of 103 litters, assignation of 369 young, heterozygosity and genetic similarity known for all marked individuals

48. Mating system I Alpine marmots Does social monogamy correspond to genetic monogamy ?

49. Within-pair litters 80.5% (83) WPY 80.7% (298) Extra-pair litters 4.9% (5) EPY 3.8% (14) Extra-pair paternity is frequent in the alpine marmot ➨ Mating system I Alpine marmots WPY 9.5% (35) Mixed litters 14.6% (15) EPY 6% (22)

50. monogamy + polyandry Mating system = Mating system I Alpine marmots Does social monogamy correspond to genetic monogamy ? Socialmonogamy  Geneticmonogamy