“Host sanctions and pollinator cheating in the fig tree-fig wasp mutualism”

1. “Host sanctions and pollinator cheating in the fig tree-fig wasp mutualism” Greg Cello and Melissa Finnell

2. About the Authors • K. Charlotte Jandér • Cornell University, Department of Neurobiology and Behavior, Ithaca • Edward Allen Herre • Biologist at the Smithsonian Tropical Research Institute • Research in co-evolution of figs and their pollinator wasps, general host- parasite co-evolution; the evolutionary effects of population structure on sex ratio, sexual selection and parasite virulence, the effects of plant pathogens on population and genetic structure if hosts, interactions between tropical host plants and both mycorrhizal and endophytic fungi.

3. Key Words • Cheaters • Individuals that reap the benefits of mutualistic interactions without paying the cost of providing service to the mutualist • Host sanctions • Mechanisms that lower the fitness of uncooperative symbionts • Foundress • Pollen-bearing female wasp • Monoecious • Species that have both male and female reproductive units

4. Key Words • Oviposition • Process of laying eggs by animals with little or no embryonic development within mother • Passive pollination • Numerous, large male flowers that release abundant pollen onto Fig wasp • Therefore, trees invest considerable resources in producing abundant pollen, and no aspect of pollen transfer relies on specialized wasp behavior • Active pollination • Relatively few, small male flowers • Pollen transfer is completely dependent on specialized wasp morphology and pollination behavior.

5. Background • Previous studies show: • Existence of host sanctions that lower fitness of uncooperative symbionts • Long-term stability of the mutualism requires mechanisms that limit or prevent cheating • Pollination is dependent on having pollen bearing female fig wasp enter fig and pollinate the flowers • Direct tradeoff between producing fig seeds or wasp offspring • Pollination syndromes in figs: • Passive • Active

6. Hypothesis • To test whether cheating levels in symbionts of fig tree-fig wasp system are related to sanction strength

7. Materials and Methods • Experimentally produced pollen carrying(P+) wasps and artificially pollen-free wasps(AP-) • Introduced one wasp into each fig to create pollinated(P+) and unpollinated(P-) figs • 2 components of fig sanctions that influence fitness: • Proportion P+ and P- figs that tree aborted • Reproductive success of AP- and P+ wasps in unaborted figs • Experimental introduction: • When figs receptive, a single AP- or P+ female wasp was introduced to random fig • Prevented uncontrolled pollination by enclosing in mesh bag

8. Materials and Methods • During weeks after introduction, aborted figs were collected • Later, non-aborted figs were collected just before wasps emerged • As wasps emerge, collected in vials and counted • Each tree produced a value of MR,OR and WR. • MR proportion of P- figs matured • OR relative number offspring in unaborted P- figs • WR relative fitness of single foundress P- wasp

9. Materials and Methods • Estimate proportion of wasps associated with each species that are likely to be single foundress • Collected unmanipulated, naturally occurring wasps to screen for “cheaters”

10. Results • Host sanctions were found in all actively pollinated fig species, but not in passively pollinated fig species • They found pollen free individuals in all species where wasps can easily cheat by omitting any of the time consuming behaviors associated with active pollination • Within these actively pollinated fig species, pollen-free wasps were most common in the species with the weakest sanctions. • The proportion of naturally occurring pollen-free wasps was negatively correlated with sanction strength (1 2 WR) across actively pollinated fig species

11. Discussion • Three novel findings: • Host sanctions vary dramatically • Existence of “cheaters” • Association between sanction strength and proportion of pollen-free wasps

12. Host sanctions vary dramatically • Host sanctions detected in all major subgenera of Fiscus • In actively pollinating species sanction strengths are similar to those reported previously • In passively pollinating species, there is no indication of host sanctions

13. Existence of “cheaters” • Pollen-free wasp species that belong to otherwise mutualistic pollinating wasp species • “Cheat” by omitting any time-consuming behaviors associated with active pollination • Effective cheaters with respect to tree’s seed production(female function) • Found in natural populations of all actively pollinating wasp species

14. Association between sanction strength and proportion of pollen-free wasps • Negatively correlated in active species • Pollen-free wasps most common in species with weakest sanctions • Fig sanctions likely to be a modification of aborting unpollinated flowers

15. Strengths and Weaknesses • Strengths • The article was organized in a clear and consistent manner • Covered most if not all questions that could have been asked while also addressing further needed studies • Weaknesses • None notable

16. Further Studies… • Further studies of the figs are needed to identify the level of precision and mechanism of sanctions, and to attempt to quantify the relative costs of sanctions across species. • Further studies of the wasps are needed to determine if naturally occurring pollen-free wasps inherit this trait from their mothers, and whether any fitness benefits of the pollen-free trait are large enough to explain its persistence despite the sanctions.

17. Review • What is the difference between passive and active pollination? • Are host sanctions found in actively pollination species or passively pollination species? • What does it mean to be a “cheater”? • What is the association between sanction strength and pollen-free wasps?

18. References Host sanctions and pollinator cheating in the fig tree–fig wasp mutualism K. Charlotte Jander and Edward Allen Herre 1 Department of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA 2 Smithsonian Tropical Research Institute, Unit 9100, PO Box 0948, DPO, AA 34002-9998, USA 3 Department of Animal Ecology, Evolutionary Biology Centre, Uppsala University, 752 36 Uppsala, Sweden