Slide 1

Actual and potential tragedies: conflicts over female caste fate in Apis and Melipona bees Tom Wenseleers & Francis Ratnieks University of Sheffield, UK Slide 2 Stingless bees Yucatan, Mexico Slide 3 Stingless bees So Paulo, Brazil Slide 4 Workers Give up reproduction for the benefit of their mother queen Darwinian puzzle The sterile worker caste of the social Hymenoptera poses one special difficulty, which at first appeared to me insuperable, and actually fatal to my whole theory. Darwin (1859) On the Origin of Species Why become a worker? Slide 5 E.g. honey bee benefit of becoming a queen: ability to head daughter swarm SO WHY DO NOT MANY FEMALES OPT TO BECOME QUEENS? females benefit from becoming a queen, but colony would suffer if all would do so caste fate conflict (colony mostly needs workers for swarming) individual benefits but collective suffers = tragedy of the commons Bourke and Ratnieks 1999 BES Slide 6 Tragedy of the commons Each individual gains by pursuing interests that increase returns relative to neighbours but decrease the value of the common goods. If all succumb to the temptation of free-riding, the outcome is a collective disaster. William Forster Lloyd 1832 Slide 7 Slide 8 Socially controlled, caste fate enforced Queen rearing in honey bees Slide 9 Exception: Melipona stingless bees Q Q Q Q Q Slide 10 Queens no larger than workers... Q Q Q Q Q Slide 11 ...in fact they are slightly smaller 66.1 mg mean = 48.2 mg mean = 57.1 mg F 3,480 =76.3, p < 1E-13 Melipona beecheii Wenseleers et al., in prep. Slide 12 Both castes reared from same cells Slide 13 Mass provisioning Slide 14 Melipona support predictions: excess queens Q Q Q Q Q Slide 15 Excess is killed Slide 16 Slide 17 Slide 18 Slide 19 Killing occurs quickly Colony% of queens in brood combs % N % of queens among adults % N Life expectancy virgin queens 4146150.35113125 hours 524210.2218438 3b185210.65122635 T1225601.5053262 T2237320.4961219 T31711840.0012730 Queens killed within 25 hours after eclosing Life expectancy adult workers = 48.5 days Melipona beecheii Slide 20 Summary social insect females benefit from developing as a queen in Melipona, females have the ability to do this (self determination) results in excess queen production why do not all females develop as a queen? what limits exploitation within the group? Slide 21 W.D. Hamilton (1936-2000) Kin selection theory Slide 22 Costs to kin can limit exploitation when selfishness causes cost to kin exploitation becomes less profitable queen overproduction causes depletion of workforce and has two costs to kin: reduced ability to swarm reduced production of males prediction: less exploitation when group members are highly related has never been tested Slide 23 Factors determining kinship multiple mating by queen: reduces relatedness among sisters does not occur in stingless bees worker laying workers can sometimes produce sons relatedness to workers sons = 0.75 relatedness to queens sons = 0.25 can occur in stingless bees Slide 24 Caste conflict model female should become a queen with a probability of (1-R f ) / (1+R m ) (self determination) with R f = sister-sister relatedness R m = relatedness to males = 20% under single mating, all males queen produced = 14% under single mating, all males worker produced assuming linear cost to total colony reproduction higher/lower ratios with other cost functions Ratnieks 2001 BES; Wenseleers & Ratnieks submitted Slide 25 Test: interspecies comparison PREDICTION less queen overproduction when males are workers sons, since costs are then to closer relatives (nephews, r = 0.75, rather than brothers, r = 0.25) Slide 26 % of males workers sons M. quadrifasciata 3 Various sites, Brazil M. subnitida 2 Rio Grande do Norte, Brazil M. beecheii 1 Yucatan, Mexico M. favosa 4 Tobago, West Indies * * 4 / 604 / OBS 4 / 1,338 / GEN+OBS 16 / 505 / GEN+OBS 13 / 108 / GEN #cols. / #males / study * GLZ, p < 10 -15 N.S. Male parentage in Melipona % of males LOW > INTERMEDIATE > HIGH workers sons 1 Paxton et al 2001; 2 Contel & Kerr 1976; Koedam et al 1999, 2002; 3 da Silva 1977; Toth et al 2002; 4 Sommeijer et al 1999 All species singly mated: Peters et al 1999, Contel & Kerr 1976, Paxton et al 2001, Kerr 1975, Kerr et al 1962 Mean, 95% C.L. Slide 27 Yucatan: Melipona beecheii Slide 28 Ah Muzencab Slide 29 Slide 30 Slide 31 M. beecheii caste ratios Prop. of queens produced Max. = 21% Average = 14.6% 10 cols. 8,162 ind. 95% C.L. Moo-Valle, Quezada-Euan and Wenseleers 2001 Insectes Sociaux Slide 32 % of queens produced % males workers 0% 34% 41% 95% sons predicted level HIGHEST > INTERMEDIATE > LOWEST of queen production M. beecheii 1 Yucatan, Mexico M. quadrifasciata 4 Various sites, Brazil M. subnitida 3 Rio Grande do Norte, Brazil M. beecheii 2 Yucatan, Mexico M. favosa 5 Tobago, West Indies * * 78 / 10 / 13,514 9 / 11 / 2,8066 / 2 / 3,989 10 / 12 / 8,162 3 / 1 / 2,476 Cols. / months / indivs. * GLZ, p < 10 -10 N.S. Test: interspecies comparison 1 Darchen & Delage-Darchen 1975; 2 Moo-Valle et al 2001; 3 Koedam et al 1999, 2002; 4 Kerr 1950; 5 Sommeijer et al 2002 Mean, 95% C.L. Slide 33 % of queens produced N.S. * * Data from months with maximum queen production only M. quadrifasciata 3 Various sites, Brazil M. subnitida 2 Rio Grande do Norte, Brazil M. beecheii 1 Yucatan, Mexico M. favosa 4 Tobago, West Indies 1 Moo-Valle et al 2001; 2 Koedam et al 1999, 2002; 3 Kerr 1950; 4 Sommeijer et al 2002 % males workers 0% 34% 41% 95% sons predicted level HIGHEST > INTERMEDIATE > LOWEST of queen production Mean, 95% C.L. * GLZ, p < 10 -10 Test: interspecies comparison Slide 34 MULTIPLE MOTHER QUEENS lowers relatedness should cause even greater queen overproduction Future test: Melipona bicolor Slide 35 Summary Melipona females selfishly exploit colony by developing as queens causes tragedy of the commons: queen overproduction reduced exploitation when costs are to close kin (workers sons) Slide 36 Alternative explanations for excess queen production in Melipona ? Slide 37 1. Kerrs theory of genetic caste determination Kerr (1950) proposed 2-locus 2-allele system for Melipona females heterozygous at both loci develop into queens results in 25% queens Slide 38 Different levels of explanation not an alternative hypothesis different level of explanation (Alcock 1993) : Kerrs hypothesis suggests HOW the observed caste ratios could come about (PROXIMATE) Caste conflict theory explains WHY the caste ratios are as observed (ULTIMATE) cf. XY-sex determination as an efficient mechanism to attain optimal 1:1 sex ratio in mammals Slide 39 2. Insurance against queen loss? queen are overproduced to ensure that continuous stock of queens is present bet-hedging argument queen overproduction is far too high queen replacement takes 10 days in this period up to 70 queens are produced there are other ways to ensure a continuous stock of queens Slide 40 Queen stocks kept in prisons In Trigonini stingless bees, e.g. Plebeia remota ensures that continuous stock of queens is present without having to overproduce them Slide 41 What about other social insects? other swarming social insects: queen-worker size dimorphism army ants honey bees trigonine (non-Melipona) stingless bees caste fate enforced via food control results in few queens being produced makes individuals work for the benefit of society and develop as a worker, even when not in best interests of individuals themselves Slide 42 Queen rearing in honey bees Policing of caste fate: food control Slide 43 Honey bee multiply mated: R f =0.3, R m =0.25 females would like to become queens with prob. of (1-R f ) / (1+R m ) = 56% only 0.02% actually become queens strong divergence between individual and colony optimum females are coerced into a working role Slide 44 Queen rearing in trigonine bees Policing of caste fate: food control Slide 45 Evasion of caste policing: dwarf queens observations occur in ants and trigonine bees same size as workers produced in excess can reproduce, although usually less fecund hypothesis selfish strategy to overcome worker feeding control? support overproduced relative to normal queens Slide 46 45 Q q q Q b c a a d d q Qw Slide 47 Plebeia remota dwarf queen normal queen 2 mm Slide 48 Frequency of dwarf queens overproduced relative to normal queens E.g. Schwarziana quadripunctata 1 in 85 worker cells (1.2%) yield dwarf queens only 1 in 620 females reared as normal queens (0.16%) i.e. 88% of all queens produced are dwarf queens & produced in 7-fold excess relative to normal queens excess queens are killed by workers as in Melipona as predicted by caste conflict theory ! Slide 49 48 Slide 50 Caste conflict in termites Slide 51 Termite caste conflict when colony loses royal pair it may be replaced by replacement reproductives (neotenics) in lower termites most individuals are totipotent any individual would like to be a replacement reproductive but just one pair is needed = another example of a ToC should result in excess production of replacements Slide 52 Termite caste conflict model ESS is to molt into a replacement reproductive with a probability of 1-relatedness = 1 0.5 = 50% cf. Frank 1995 (assuming outbreeding) predicts development of excess replacements Wenseleers, Korb & Ratnieks, in prep. Slide 53 Cryptotermes brevis 50% of all individuals develop as neotenics (Lenz et al. 1985) all but one pair killed as predicted by caste conflict theory Slide 54 Development and killing of excess reproductives TERMOPSIDAEPorotermes adamsoniMensa-Bonsu 1976 Lenz 1985 KALOTERMITIDAEKalotermes flavicollisRuppli 1969, Lscher 1952, 1956, 1974 Neotermes connexusMyles & Chang 1984 Neotermes jouteliNagin 1972 Cryptotermes brevisLenz et al. 1985 RHINOTERMITIDAEReticulitermes lucifugusBuchli 1956 Reticulitermes santonensis Wenseleers, Korb & Ratnieks, in prep. Slide 55 Summary social insect caste system provides scope for conflict caste conflict may cause significant costs to the society (Melipona queen overproduction) coercion is more effective than kinship in suppressing caste conflict Slide 56 What can we learn from all this? Slide 57 Insight into conflict resolution Self determination 20% queen production stingless bees Policing of caste fate 0.02% queen production honey bees Individual Freedom Causes a Cost to Society But females prefer to become queen with probability of 56% ! Efficient Society but No Individual Freedom THE SAME TENSION OCCURS IN HUMAN SOCIETY ! Slide 58 Bourke A.F.G., Ratnieks F.L.W. 1999. Kin conflict over caste determination in social Hymenoptera. Behavioral Ecology & Sociobiology 46: 287-297. Moo-Valle H., Quezada-Eun J.J.G., Wenseleers T. 2001. The effect of food reserves on the production of sexual offspring in the stingless bee Melipona beecheii (Apidae, Meliponini). Insectes Sociaux 48: 398-403. Ratnieks F.L.W., Monnin T., Foster K.R. 2001. Inclusive fitness theory: novel predictions and tests in eusocial Hymenoptera. Annales Zooogici Fennici 38: 201- 214. Ratnieks F.L.W. 2001. Heirs and spares: caste conflict and excess queen production in Melipona bees. Behavioral Ecology & Sociobiology 5: 467-473. Wenseleers T., Ratnieks F.L.W., Billen J. 2002. Conflict over caste fate in social insects: a tragedy of the commons examined. Submitted. Wenseleers T., Ratnieks F.L.W. 2002. Tragedy of the commons in bees. Submitted. PDF reprints and talk at www.shef.ac.uk/projects/taplab/twpub.html References Slide 59 Acknowledgements Collaborators V-L. Imperatriz-Fonseca, M. de F. Ribeiro, D. de A. Alves (SP, Brazil) H. Moo-Valle, J. Quezada-Eun and Luis Medina-Medina (Dept. of Apiculture, Merida, Mexico) R. Paxton (Tbingen, Germany) Funding British Council FWO-Vlaanderen Vlaamse Leergangen EU INSECTS and Social Evolution Networks Marie Curie Fellowship