1. The effect of relatedness on the evolution of altruism in insect societies Tom Wenseleers Laboratory of Entomology University of Leuven, Belgium tom.wenseleers@bio.kuleuven.be

2. Hamilton’s rule -altruism favoured when B.r > C -predicts that high relatedness and low cost/benefit ratio should lead to more altruism -data from cooperatively breeding birds & mammals support this, but what about social insects? white-fronted bee eater Seychelles warbler pied kingfisher Beldings ground squirrel

3. Altruism in social insects -can take several forms: in the context of the origin of eusociality: decision for a female not to mate but help in advanced eusocial species: decision for a larva to develop as a worker decision for a worker not to lay eggs & remain sterile - I tested the role of relatedness in these last 2 contexts

4. 1. Develop as a worker QUEEN SELFISH OPTION WORKER ALTRUISTIC OPTION Bourke & Ratnieks 2001 Beh. Ecol. Sociob.; Wenseleers et al. 2003 J. Evol. Biol. female larva Prediction: when relatedness is high, a higher proportion of the larvae are selected to altruistically develop as workers rather than queens

5. Empirical test -usually the choice to become either a queen or a worker is out of the hands of the developing larvae -but not in Melipona stingless bees: queens and workers same size and reared in identical cells -prediction: male production by workers increases the relatedness to the males reared and should increase the % that develop as workers Wenseleers et al. 2003 J. Evol. Biol.

6. Q Q Q Q Q % queens reared determined by uncapping cells

7. Prediction supported greater altruism (more develop as workers) when more of the males are workers’ sons (higher r) supports role of kinship in influencing decision to become queen or worker Pearson R=-0.89, p=0.02 increased relatedness to males reared increased altruism Wenseleers & Ratnieks 2004 Proc. R. Soc. B

8. 2. Worker sterility worker LAY MALE EGGS SELFISH OPTION REMAIN STERILE ALTRUISTIC OPTION

9. Theoretical predictions Increased worker altruism and a decreased tendency to reproduce directly is favoured when it satisfies Hamilton’s rule, c < b.r, i.e. when relatedness is high ORthere is a low cost of not reproducing (low c/b): this is the case if worker reproduction is more effectively policed by nestmates (small cost of not laying eggs if they would be eaten anyway) Which of these two factors has the dominant effect? Wenseleers et al. 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat.

10. - compiled data set of 10 species with good data on relatedness, effectiveness of policing and % of reproductive workers (9 Vespidae wasps + honeybee) - combination of own + literature data Empirical test

11. Empirical data: opposite to Hamiltonian scenario more workers reproduce when relatedness is high ! high relatedness leads to less altruism ! 0.30.40.50.60.7 relatedness among workers 0.075 0.25 0.5 0.75 2.5 5 7.5 25 % of reproductive workers Polistes chinensis Apis mellifera Vespula germanica Vespa crabro D. media Vespula rufa Dolichovespula saxonica Vespula vulgaris D. norwegica D. sylvestris 0.30.40.50.60.7 relatedness among workers 0.075 0.25 0.5 0.75 2.5 5 7.5 25 % of reproductive workers Polistes chinensis Apis mellifera Vespula germanica Vespa crabro D. media Vespula rufa Dolichovespula saxonica Vespula vulgaris D. norwegica D. sylvestris Pearson R=0.82, p=0.004 Wenseleers & Ratnieks submitted

12. more effective policing  fewer workers reproduce also significant if phylogenetic non-independence is controlled for Effective policing favours worker sterility effectiveness of policing (%) 1009998959080705030 0 5 10 30 % of reproductive workers Polistes chinensis D. sylvestris D. norwegica D. media Apis mellifera Vespula rufa Dolichovespula saxonica Vespa crabro Vespula germanica Vespula vulgaris PearsonR=-0.94,p=0.00004 Wenseleers & Ratnieks submitted

13. Ratnieks 1988 Am. Nat. Why does low relatedness lead to more cooperation? when relatedness is low (r < 0.5) workers are more highly related to queen’s sons (r=0.25) than to other workers’ sons (r<0.25) this favours workers to police each others’ eggs, and this in turn reduces the benefit for workers to lay eggs in the first place

14. Direct and indirect effects of relatedness - in other words, relatedness has a dual effect: direct effect high relatedness favours fewer workers to lay eggs indirect effect low relatedness favours policing and this should favour fewer workers to lay eggs - data show that the indirect effect of relatedness is the most important - what about worker reproduction in queenless colonies, where policing does not occur – direct effect of relatedness? Wenseleers et al. 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat.

15. In queenless colonies: high relatedness promotes altruism fewer workers reproduce when relatedness is high conforms to basic Hamiltonian prediction Apis mellifera Vespula vulgaris Vespula germanica Vespa crabro Dolichovespula media Dolichovespula norwegica Dolichovespula sylvestris Dolichovespula saxonica Vespula rufa Polistes chinensis 0.30.40.50.60.7 0 5 10 15 20 25 30 35 40 % of reproductive workers relatedness among workers Pearson R=-0.79, p=0.007 Wenseleers & Ratnieks submitted

16. Evidence that low relatedness selects for worker policing? worker policing expected when relatedness is low evidence for this controversial; several examples support prediction (e.g. honey bee, r=0.3), others not (e.g. hornet) solution: meta-analysis of own+literature data predictions: when relatedness is low worker policing should be more common % of males that are workers’ sons should be lower Wenseleers & Ratnieks 2006 Am. Nat.

17. Lasioglossum zephyrum Bombus agrorum Bombus ardens Bombus bifarius Bombus ephippiatus Bombus hypocrita Bombus impatiens Bombus lapidarius Bombus ruderatus Bombus terrestris Melipona bicolor Melipona compressipes Melipona favosa Melipona subnitida Melipona scutellaris Paratrigona subnuda Scaptotrigona depilis Scaptotrigona postica Apis florea Apis cerana Apis mellifera Apis mellifera capensis Polistes biglumis Polistes chinensis Polistes dominulus Vespa crabro gribodi Dolichovespula maculata Dolichovespula media Dolichovespula arenaria Dolichovespula saxonica Dolichovespula norwegica Dolichovespula sylvestris Vespula rufa Vespula vulgaris Vespula germanica Diacamma sp. Dinoponera quadriceps Pachycondyla inversa Platythyrea punctata Camponotus floridanus Formica fusca Crematogaster smithi Harpagoxenus sublaevis Leptothorax acervorum Protomognathus americanus Leptothorax unifasciatus Microstigmus comes Augochlorella striata Lasioglossum malachurum Lasioglossum laevissimum Lasioglossum zephyrum Bombus terrestris Bombus hypnorum Bombus melanopygus Tetragona clavipes Trigona carbonaria Trigona clypearis Trigona hockingsi Trigona mellipes Plebeia droryana Plebeia remota Plebeia saiqui Schwarziana quadripunctata Melipona beecheii Melipona favosa Melipona marginata Melipona quadrifasciata Melipona scutellaris Melipona subnitida Paratrigona subnuda Scaptotrigona postica Austroplebeia australis Austroplebeia symei Apis dorsata Apis florea Apis cerana Apis mellifera Polistes chinensis Polistes gallicus Polistes dorsalis Polistes bellicosus Polistes fuscatus variatus Polistes metricus Polybioides tabidus Brachygastra mellifica Parachartergus colobopterus Vespa ducalis Vespa mandarinia Vespa crabro flavofasciata Vespa crabro gribodi Dolichovespula maculata Dolichovespula media Dolichovespula arenaria Dolichovespula saxonica LP Dolichovespula saxonica HP Dolichovespula norwegica Dolichovespula sylvestris Vespula rufa Vespula squamosa Vespula germanica Vespula maculifrons Vespula vulgaris Dinoponera quadriceps Dorylus molestus Iridomyrmex purpureus Rhytidoponera chalybaea Rhytidoponera confusa Colobopsis nipponicus Camponotus ocreatus Lasius niger Formica fusca Formica rufa Formica truncorum Formica exsecta Formica sanguinea Polyergus rufescens Nothomyrmecia macrops Crematogaster smithi Harpagoxenus sublaevis Leptothorax acervorum Leptothorax allardycei Epimyrma ravouxi Leptothorax nylanderi Leptothorax unifasciatus Protomognathus americanus Aphaenogaster carolinensis Myrmica punctiventris Myrmica tahoensis Myrmica ruginodis Pogonomyrmex rugosus Cyphomyrmex costatus Cyphomyrmex longiscapus Sericomyrmex amabilis Trachymyrmex cf zeteki Trachymyrmex cometzi sp1 Acromyrmex echinatior Acromyrmex octospinosus Acromyrmex echinatior Aphaenogaster smythiesi sweat bees bumblebees stingless bees honeybees Polistinae Vespinae ants bees wasps Sphecid wasps sweat bees bumblebees st. bees honeybees Polistini Epiponini Polistinae wasps Vespinae ants behavioural evidence male parentage n=48 speciesn=90 species red: worker policing predicted orange: worker policing neutral Wenseleers & Ratnieks 2006 Am. Nat.

18. Analysis behavioural studies worker policing present in all species (7/7) where it is predicted based on relatedness worker policing absent in most (27/34=79%) other species difference highly significant (p=0.0002), also if phylogenetic non-independence is controlled for (p<0.001) Wenseleers & Ratnieks 2006 Am. Nat.

19. Analysis of male parentage n=90 species t-test, p=0.0000000001 after controlling for phylogenetic nonindependence: p=0.02-0.000003

20. Summary - high relatedness can promote altruism: higher proportion of Melipona larvae that develop as workers higher proportion of the workers that remain sterile in queenless colonies - but sanctions / policing also important, and this can override the basic Hamiltonian relatedness prediction

21. Thanks to… D. Alves, V. Imperatriz-Fonseca, J. Quezada, M. Ribeiro A. Tofilski, F. Nascimento, K. Vuerinckx, J. Billen M. Archer, N. Badcock, T. Burke, K. Erven A. Hart, H. Helantera Francis RatnieksKevin Foster