Why do females mate with multiple males?

1. Why do females mate with multiple males?

2. Appear to be monogamous. Are they? Lazuli Bunting (Erick Greene)

3. Not Dad’s... most birds are socially monogamous yet we find extra-pair young in ~ 75% of species Nope! typically 25-60% of nests have extra-pair young

4. Splendid fairy-wren (Australia): highly social, cooperatively-breeding bird. Highest known extra-pair fertilization rate (~60%).

5. ! DNA microsatellite ~ Box 11.1 Alcock

6. History of research on extra-pair mating • Behavioral studies reveal mate guarding • Explanation focuses on male perspective • Molecular studies reveal extra-pair parentage • Explanation shifts focus to female perspective • Research shifts back to behavior

7. Bank Swallow (Sand Martin)

8. on the Columbia ~ 1000 pairs bank swallows: make burrows in sand banks, nest at back

9. A small bank swallow colony (~100 nests) in the Palouse

10. Mate Guarding

11. Mate Guarding

12. Mate Guarding

13. Mate Guarding

14. This looks like rape but it isn’t (for one thing this is a dead bird, ugh). The more important point is that a male songbird cannot forceably mate a female – she has to cooperate for insemination to occur. This is true for many animals, including many mammals. Extra-pair mating is common in songbirds but rape is not.

16. Male’s mixed reproductive strategy: • Guard your mate • Pursue extra-pair copulations rest of the time, until • (3) Kids hatch, then go into parental mode

17. Male Perspective: a ‘Mixed’ Reproductive Strategy Male bank swallow follows a ‘mixed’ reproductive strategy – he mates monogamously but while mate is incubating the eggs, he pursues promiscious (extra-pair) matings with other females (Beecher & Beecher 1979).

18. 20 years later: Molecular data on Sand Martins (Bank Swallows) – DNA Fingerprinting (Alves & Bryant 1998) Parentage % offspring Social parents 81.4 Extra-pair fertilization* 14.4 Intra-specific parasitism** 1.8 * Social Dad is not Genetic Dad ** Neither social parent is genetic parent

19. The Mating Game (at least) three players • The female • Her social mate • The extra-pair mate

20. Should I sneak out or mate guard?... Where is she anyway? Male Perspective • Winners: +1 offspring • Losers: -1 offspring • Net benefit = epfs you gain minus epfs you lose • Classic trade-off situation • Do I mate guard? • Or pursue extra-pair copulations (EPCs)?

21. Female Perspective Benefits & costs less obvious • Direct benefits: food, protection, making sure eggs get fertilized • Indirect benefits:Good genes, compatible genes, inbreeding avoidance • Benefits imply female pursuit of EPM

22. What are the possible reasons for a ‘monogamous’ female to mate with ‘extra-pair’ males? • Her social mate has below-average genetic quality • Her social mate is sterile • She wants additional help or resources for her kids • Her social mate has incompatible genes • She wants genetic diversity in her offspring • She wants to confuse everyone about who’s the father* *relates to multiple mating but not to the social monogamy + shared P.C. case

23. What are the possible reasons for a ‘monogamous’ female to mate with ‘extra-pair’ males? • Her social mate has below-average genetic quality • Her social mate is sterile • She wants additional help or resources for her kids • Her social mate has incompatible genes • She wants genetic diversity in her offspring • She wants to confuse everyone about who’s the father* Anti-infanticide mechanism? Popular hypothesis re multi-male primate groups (chimps, baboons, others) *relates to multiple mating but not to the social monogamy + shared P.C. case

24. What are the possible reasons for a ‘monogamous’ female to mate with ‘extra-pair’ males? • Her social mate has below-average genetic quality • Her social mate is sterile • She wants additional help or resources for her kids • Her social mate has incompatible genes • She wants genetic diversity in her offspring • She wants to confuse everyone about who’s the father* Same argument as the Good Genes argument in sperm-only species *relates to multiple mating but not to the social monogamy + shared P.C. case

25. What are the possible reasons for a ‘monogamous’ female to mate with ‘extra-pair’ males? • Her social mate has below-average genetic quality • Her social mate is sterile • She wants additional help or resources for her kids • Her social mate has incompatible genes • She wants genetic diversity in her offspring • She wants to confuse everyone about who’s the father* Similar argument to the argument for why sexual reproduction beats asexual reproduction *relates to multiple mating but not to the social monogamy + shared P.C. case

26. What are the possible reasons for a ‘monogamous’ female to mate with ‘extra-pair’ males? • Her social mate has below-average genetic quality • Her social mate is sterile • She wants additional help or resources for her kids • Her social mate has incompatible genes • She wants genetic diversity in her offspring • She wants to confuse everyone about who’s the father* outbreeding > inbreeding *relates to multiple mating but not to the social monogamy + shared P.C. case

27. Splendid fairy-wren (Australia): highly social, cooperatively-breeding bird. Highest known extra-pair fertilization rate (~60%). Limited dispersal in this species. Inbreeding is a potential problem.

28. An example: the Splendid Fairy-Wren (Tarvin et al 2005) None Mixed Complete Level of extrapair paternity in the brood (a) When young are all EPY, female is more genetically similar to her social mate than to the average male. (b) But female’s extra-pair mate is not more genetically dissimilar than the average male. Suggests that choice is made post-copulation, and that it serves inbreeding avoidance.

29. Crypic Female Choice PRE copulation POST Sperm Competition Male-male Competition Female Choice Cryptic Female Choice When there is multiple mating and internal fertilization, male-male competition and female choice do not stop at copulation, but continue in the female reproductive tract as sperm competition and “cryptic female choice”. Cryptic female choice = the ability of female to control which sperm reaches her eggs during and after the mating process.

30. Crypic Female Choice

31. Crypic Female Choice

32. Female Perspective Cryptic female choice implies a new hypothesis: Any Dude will Do! “Red Rooster says ‘Cock-a-doodle-doo’ Richland Woman says ‘Any dude will do’”* *Richland Woman Blues (Mississippi John Hurt)

33. Female Perspective ‘Good genes’ female choice implies • female will choose extra-pair male on basis of honest signals of male quality (e.g., big song repertoire) • Female will only extra-pair mate if she can ‘mate up’

34. Who drives extra-pair mating? ? ? Does E-P male foray onto female’s territory? Or she onto his?

35. Back to behavior: Radio-tracking pairs There goes our privacy… • We need data on both the male and female behavior, ideally at the same time • Why radio-tracking? • Females are less conspicuous • Both the male and the female are expected to be inconspicuous outside the territory (females are much more so)

37. What are the possible reasons for a ‘monogamous’ female to mate with ‘extra-pair’ males? • Her social mate has below-average genetic quality • Her social mate is sterile • She wants additional help or resources for her kids • Her social mate has incompatible genes • She wants genetic diversity in her offspring • She wants to confuse everyone about who’s the father* *relates to multiple mating but not to the social monogamy + shared P.C. case

38. Why do females mate with multiple males? Splendid Fairy-wren

39. Bet-hedging hypothesis: multiple mating decreases variance in RS and hence increases the geometric mean fitness when there are mate choice and/or environmental uncertainties. A = arithmetic mean = (X1 + … + XN) / N G = geometric mean = (X1∙ … ∙ XN) 1/N G=A–2/2

40. What are the possible reasons for a ‘monogamous’ female to mate with ‘extra-pair’ males? • She wants additional help or resources for her kids • Her social mate is sterile • Her social mate has below-average genetic quality • Her social mate has incompatible genes • She wants genetic diversity in her offspring • She wants to confuse everyone about who’s the father* direct benefits good genes *relates to multiple mating but not to the social monogamy + shared P.C. case

41. Male bank swallow courts female

42. Extra-pair mating (EPM) in birds • Most birds are socially monogamous • Strong pair-bond • Biparental care • But most are not genetically monogamous • Females (males) mate with males (females) other than their social mate