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The effect of relatedness on the evolution of altruism in insect societies

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. Hamilton’s rule . altruism favoured when B . r > C

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The effect of relatedness on the evolution of altruism in insect societies

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  1. The effect of relatedness on the evolution of altruism in insect societies Tom WenseleersLaboratory of EntomologyUniversity 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 workerdecision 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 female larva WORKER ALTRUISTICOPTION QUEEN SELFISHOPTION Prediction: when relatedness is high, a higher proportion of the larvae are selected to altruistically develop as workers rather than queens Bourke & Ratnieks 2001 Beh. Ecol. Sociob.; Wenseleers et al. 2003 J. Evol. Biol.

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

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

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

  8. 2. Worker sterility worker REMAIN STERILE ALTRUISTICOPTION LAY MALE EGGS SELFISHOPTION

  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 OR there 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. Empirical test • 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

  11. Empirical data: opposite to Hamiltonian scenario more workersreproduce when relatedness is high ! high relatedness leads to less altruism ! Polistes chinensis Polistes chinensis 25 25 Dolichovespula saxonica Dolichovespula saxonica D. sylvestris D. sylvestris Vespula rufa Vespula rufa 7.5 7.5 D. norwegica D. norwegica 5 5 D. media D. media 2.5 2.5 Vespula germanica Vespula germanica Vespa crabro Vespa crabro % of reproductive workers % of reproductive workers 0.75 0.75 Vespula vulgaris Vespula vulgaris 0.5 0.5 0.25 0.25 0.075 0.075 Pearson R=0.82, p=0.004 Apis mellifera Apis mellifera 0.3 0.3 0.4 0.4 0.5 0.5 0.6 0.6 0.7 0.7 relatedness among workers relatedness among workers Wenseleers & Ratnieks submitted

  12. Effective policing favours worker sterility more effective policing  fewer workers reproduce also significant if phylogenetic non-independence is controlled for Pearson R = - 0.94, p =0.00004 Polistes chinensis 30 Dolichovespula saxonica % of reproductive workers 10 Vespula rufa D. sylvestris D. norwegica D. media 5 Vespa crabro Vespula germanica Vespula vulgaris 0 Apis mellifera 30 50 70 80 90 95 98 99 100 effectiveness of policing (%) Wenseleers & Ratnieks submitted

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

  14. Direct and indirect effects of relatedness • - in other words, relatedness has a dual effect: • direct effect high relatedness favours fewer workers to lay eggsindirect 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 40 fewer workersreproduce when relatedness is high conforms to basicHamiltonian prediction Apis mellifera 35 Vespula germanica Vespula vulgaris 30 Polistes chinensis 25 Vespula rufa % of reproductive workers 20 Dolichovespula sylvestris 15 Vespa crabro Dolichovespula saxonica 10 Dolichovespula media Dolichovespula norwegica 5 Pearson R=-0.79, p=0.007 0 0.3 0.4 0.5 0.6 0.7 relatedness among workers Wenseleers & Ratnieks submitted

  16. Evidence that low relatedness selectsfor 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 lowworker policing should be more common% of males that are workers’ sons should be lower Wenseleers & Ratnieks 2006 Am. Nat.

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

  18. Analysis behavioural studies • worker policingpresent 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 t-test, p=0.0000000001 after controllingfor phylogeneticnonindependence: p=0.02-0.000003 n=90 species Wenseleers & Ratnieks 2006 Am. Nat.

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

  21. Thanks to… Francis Ratnieks Kevin Foster • 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

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