Possible links between sexual-system evolution and demographic processes in plants and animals

1. Possible links between sexual-system evolution and demographic processes inplants and animals John Pannell Department of Plant Sciences University of Oxford

3. (Male-sterility) Gynodioecy Hermaphroditism Androdioecy (Female-sterility)

4. Maintaining males versus females Frequency of males or females Relative production of seeds or pollen (relative to hermaphrodites)

5. Maintaining males versus females Gynodioecy under selfing & inbreeding depression Frequency of males or females Relative production of seeds or pollen (relative to hermaphrodites)

6. Maintaining males versus females Gynodioecy under selfing & inbreeding depression Frequency of males or females Androdioecy under selfing & inbreeding depression Relative production of seeds or pollen (relative to hermaphrodites)

7. In fact… • Androdioecy has evolved several times • Males typically occur with partially selfing hermaphrodites Predictions • Androdioecy should be difficult to evolve • Androdioecy should occur only where hermaphrodites are prevented from selfing

8. Occurrence of androdioecy Datisca glomerata Mercurialis annua Schizopeponbryoniaefolius Kryptolebias marmoratus

9. Several species of branchiopod crustaceans Herm Male Sassaman, 1995 Steve Weeks

10. Several species of the Oleaceae Wallander, 2001

11. Mercurialis annua Durand (1963)

12. reduced selfing population growth Colonisation hermaphroditesselected with female-biased sex allocation Immigration malesselected males hermaphrodites Established population

13. Within-population diversity Pair-wise differentiation Obbard, Harris & Pannell (Am Nat, 2006)

14. Males present Males absent • 445 populations • 5 transitions in breeding system • 3 years of demographic sampling

15. Males + females Hermaphrodites Dorken & Pannell (2007: Heredity)

16. Males present Males absent 7000 6000 5000 4000 Abundance (number of plants) 3000 2000 1000 0 40 50 60 70 80 90 100 Occupancy (% occupied sites) Eppley & Pannell (2006: American Naturalist)

17. 49/185 25/171 Males present Males absent Dorken, Freckleton & Pannell (unpublished data)

18. 6x 2x Monoecy Dioecy (Central) Dioecy (West) Monoecy Androdioecy Dioecy (East) Obbard, Harris & Pannell (American Naturalist, 2006)

19. 6x Monoecy Dioecy (Central) Dioecy (West) Monoecy Androdioecy Dioecy (East) Is there less inbreeding depression in northern populations of M. annua?

20. Pujol et al. (PNAS, 2009)

21. 6x Is there less quantitative genetic variation for sex allocation in northern populations of M. annua? Monoecy Dioecy (Central) Dioecy (West) Monoecy Androdioecy Dioecy (East)

22. Pujol and Pannell (2008, Science)

23. males hermaphrodites hermaphrodites Frequency 0.0 Sex allocation 1.0

24. Nutrient status Malefrequency

25. Dorken and Pannell (Current Biology, in press)

26. Durand (1963)

27. Selfing rates in different patches Without males With males Korbecka and Pannell, unpubl.

28. Dorken, Freckleton & Pannell (unpublished data) Eppley and Pannell (2008: Evolution)

29. Herm Male Occurrence of males with hermaphrodites Datisca glomerata Eulimnadia texana Schizopeponbryoniaefolius Kryptolebias marmoratus Caenorhabditis elegans

30. Hermaphrodites Weeks et al. (2006) Males + hermaphrodites 24–180 million years ago Males + females Herm Males and hermaphrodites in Eulimnadia species Male

31. Why is androdioecy in Eulimnadia so ancient? Hermaphrodites are the heterogametic sex W/Z Z/Z

32. W/Z Z/Z • Deleterious recessives on W • NOT expressed • FIXED by drift • Selection for reproductive assurance • Females produce an ovotestis • Androdioecy evolves W/Z Z/Z • Selfing produces homozygous W • Load on W now expressed • Fitness of W/W < W/Z W/W W/Z

33. Maintenance of males  = 0.9  = 0.9 • = 0 (no recessive load on W)  = 0.1 Male frequency  = 0.9  = 0.5 • > 0 (recessive load on W)  = 0.1 (recessive load on W) Probability of finding a mate

34. Maintenance of males  = 0.9  = 0.9 • = 0 (no recessive load on W)  = 0.1 Male frequency  = 0.9  = 0.5 • > 0 (recessive load on W)  = 0.1 Probability of finding a mate Pannell (2008: Genetical Research)

35. Males maintained by overdominance? • ZZ males: low fitness • can’t find a mate • WW hermaphrodites: low fitness • reproductive assurance • BUT recessive genetic load on W chromosome • WZ hermaphrodites: high fitness • reproductive assurance • AND sheltering of genetic load on W chromosome

36. Fraxinus ornus • Oleaceae family • Dioecy & androdioecy are frequent in genus and family Verdu, Montilla & Pannell (Proc. Royal Soc., B, 2004)

37. 1:1 sex ratio Implies cryptic dioecy • Hermaphrodites do sire seeds Implies androdioecy Functional Ecology (2002): 16: 858-869 Proc. Royal Soc., B (2004): 271: 2017-2023 Evolution (2006) First puzzle… • Males and hermaphrodites co-occur Implies androdioecy Fraxinus ornus

38. mother father mother father Male-sired seedlings grow 8% faster than hermaphrodite-sired seedlings Proc. Royal Soc., B (2004): 271: 2017-2023

39. Hermaphrodites can be fathers but not grandfathers Hermaphrodites are functionally female Fraxinus ornus Proc. Royal Soc., B (2004): 271: 2017-2023 Evolution (2006)

40. Second puzzle… • Females produce lots of pollen… Why? M F M F Intense competition in the seed shadow Fraxinus ornus

41. Rival’s seedlings are less competitive ESS: all females invest up to 50% of reproductive resources in pollen Pannell (unpubl.) Second puzzle… • Females produce lots of pollen… Why? M F M F Intense competition in the seed shadow Fraxinus ornus

42. Third puzzle… • What is the mechanism of sabotage?

43. Thanks to… • Darren Obbard • Richard Buggs • Stephen Harris • Sarah Eppley • Marcel Dorken • Paul Rymer • Rob Freckleton • Grazyna Korbecka • Stephen Weeks • … and many undergraduate assistants NERC Royal Society BBSRC European Union