the effect of relatedness on the evolution of altruism in insect societies tom wenseleers laboratory...

The effect of relatedness on the evolution of altruism in

insect societies

Tom WenseleersLaboratory of Entomology

University of Leuven, Belgium

[email protected]

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

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

1. Develop as a worker

QUEEN

SELFISHOPTION

WORKER

ALTRUISTICOPTION

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

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.

Q

Q

Q

Q Q

% queens reared determined by uncapping cells

Prediction supported

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

0 20 40 60 80 100

% of males that are workers' sons

0

2

4

6

8

10

12

14

16

18

% o

f fem

ales

rea

red

as q

ueen

s M. beecheii

M. quadrifasciataM. marginata

M. scutellarisM. subnitida

M. favosa

Pearson R=-0.89, p=0.02

increased relatedness to males reared

incre

as

ed altru

ism

Wenseleers & Ratnieks 2004 Proc. R. Soc. B

2. Worker sterility

worker

LAY MALE EGGS

SELFISHOPTION

REMAIN STERILE

ALTRUISTICOPTION

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 beeaten anyway)

Which of these two factors has the dominant effect?

Wenseleers et al. 2004 J. Evol. Biol.; Wenseleers et al. 2004 Am. Nat.

- 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

Empirical data: opposite to Hamiltonian scenario

more workersreproduce when relatedness is high !

high relatedness leads to less altruism !

0.3 0.4 0.5 0.6 0.7

relatedness among workers

0.075

0.25

0.50.75

2.5

57.5

25

% o

f re

prod

uctiv

e w

orke

rs

Polistes chinensis

Apis mellifera

Vespula germanica Vespa crabro

D. media

Vespula rufa

Dolichovespula saxonica

Vespula vulgaris

D. norwegica

D. sylvestris

0.3 0.4 0.5 0.6 0.7


0.075

0.25

0.50.75

2.5

57.5

25

% o

f re

prod

uctiv

e w

orke

rs

Polistes chinensis

Apis mellifera

Vespula germanica Vespa crabro

D. media

Vespula rufa


Vespula vulgaris

D. norwegica

D. sylvestris

Pearson R=0.82, p=0.004

Wenseleers & Ratnieks submitted

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

% o

f rep

rodu

ctiv

e w

orke

rs Polistes chinensis

D. sylvestris

D. norwegica

D. media

Apis mellifera

Vespula rufa


Vespa crabro

Vespula germanicaVespula vulgaris

Pearson R=-0.94, p=0.00004


Ratnieks 1988 Am. Nat.

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

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.

In queenless colonies: high relatedness promotes altruism

fewer workersreproduce when relatedness is high

conforms to basicHamiltonian prediction

Apis mellifera

Vespula vulgarisVespula germanica

Vespa crabro

Dolichovespula media

Dolichovespula norwegica

Dolichovespula sylvestris


Vespula rufa

Polistes chinensis

0.3 0.4 0.5 0.6 0.70

5

10

15

20

25

30

35

40

% o

f re

prod

uctiv

e w

orke

rs


Pearson R=-0.79, p=0.007


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.

Lasioglossum zephyrumBombus agrorumBombus ardensBombus bifariusBombus ephippiatusBombus hypocritaBombus impatiensBombus lapidariusBombus ruderatusBombus terrestrisMelipona bicolorMelipona compressipesMelipona favosaMelipona subnitidaMelipona scutellarisParatrigona subnudaScaptotrigona depilisScaptotrigona posticaApis floreaApis ceranaApis melliferaApis mellifera capensisPolistes biglumisPolistes chinensisPolistes dominulusVespa crabro gribodiDolichovespula maculataDolichovespula mediaDolichovespula arenariaDolichovespula saxonicaDolichovespula norwegicaDolichovespula sylvestrisVespula rufaVespula vulgarisVespula germanicaDiacamma sp.Dinoponera quadricepsPachycondyla inversaPlatythyrea punctataCamponotus floridanusFormica fuscaCrematogaster smithiHarpagoxenus sublaevisLeptothorax acervorumProtomognathus americanusLeptothorax unifasciatus

Microstigmus comesAugochlorella striataLasioglossum malachurumLasioglossum laevissimumLasioglossum zephyrumBombus terrestrisBombus hypnorumBombus melanopygusTetragona clavipesTrigona carbonariaTrigona clypearisTrigona hockingsiTrigona mellipesPlebeia droryanaPlebeia remotaPlebeia saiquiSchwarziana quadripunctataMelipona beecheiiMelipona favosaMelipona marginataMelipona quadrifasciataMelipona scutellarisMelipona subnitidaParatrigona subnudaScaptotrigona posticaAustroplebeia australisAustroplebeia symeiApis dorsataApis floreaApis ceranaApis melliferaPolistes chinensisPolistes gallicusPolistes dorsalisPolistes bellicosusPolistes fuscatus variatusPolistes metricusPolybioides tabidusBrachygastra mellificaParachartergus colobopterusVespa ducalisVespa mandariniaVespa crabro flavofasciataVespa crabro gribodiDolichovespula maculataDolichovespula mediaDolichovespula arenariaDolichovespula saxonica LPDolichovespula saxonica HPDolichovespula norwegicaDolichovespula sylvestrisVespula rufaVespula squamosaVespula germanicaVespula maculifronsVespula vulgarisDinoponera quadricepsDorylus molestusIridomyrmex purpureusRhytidoponera chalybaeaRhytidoponera confusaColobopsis nipponicusCamponotus ocreatusLasius nigerFormica fuscaFormica rufaFormica truncorumFormica exsectaFormica sanguineaPolyergus rufescensNothomyrmecia macropsCrematogaster smithiHarpagoxenus sublaevisLeptothorax acervorumLeptothorax allardyceiEpimyrma ravouxiLeptothorax nylanderiLeptothorax unifasciatusProtomognathus americanusAphaenogaster carolinensisMyrmica punctiventrisMyrmica tahoensisMyrmica ruginodisPogonomyrmex rugosusCyphomyrmex costatusCyphomyrmex longiscapusSericomyrmex amabilisTrachymyrmex cf zetekiTrachymyrmex cometzi sp1Acromyrmex echinatiorAcromyrmex octospinosus

Acromyrmex echinatiorAphaenogaster smythiesi

sweat bees

bumblebees

stinglessbees

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 species n=90 species

red: worker policing predictedorange: worker policing neutral


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)



-0.15 -0.10 -0.05 0.00 0.05 0.10 0.15

% o

f m

ales

wor

kers

‘son

s

relatedness difference betweenworkers' and queen's sons

0

1

10

100

workers more related to queen's sons

ANTSBEESWASPS

-0.15 -0.10 -0.05 0.00 0.05 0.10 0.15

% o

f m

ales

wor

kers

‘son

s

relatedness difference betweenworkers' and queen's sons

0

1

10

100

workers more related to queen's sons

ANTSBEESWASPS

Analysis of male parentage

n=90 species

t-test, p=0.0000000001

after controllingfor phylogeneticnonindependence:p=0.02-0.000003

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

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 Ratnieks Kevin Foster

the effect of relatedness on the evolution of altruism in insect societies tom wenseleers laboratory...

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