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ANTIMICROBIALS AND THE EVOLUTION OF EUSOCIALITY

Andrew Beattie

Christine Turnbull

Department of Biological Sciences

Macquarie University

Sydney, Australia

andrew.beattie@mq.edu.au

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The major social insectsAnts (© Ron Oldfield)

Social wasps©Micropolitan.org

Social bees ©2008 Peter Owww.aussiebee.com.au

Termiteswww.evergreenpest.com.au

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Criteria for Eusociality1. Cooperative brood care2. Reproductive division of labour;

castes3. Overlap between at least two generations; offspring assist

parents4. Is there another one?

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THIS TALK

•Bull ants•Bees•Wasps•Thrips•(Bioprospecting)

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Bull Ants have two defences against antimicrobial attack

1. EXTERNAL• Paired metapleural

glands• Strong antiseptic

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Extracting antimicrobial metapleural secretions

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Metapleural secretion activity against microorganisms

Yeasts (fungi):strong

Gram + bacteria:mixed

Gram –ve: strong

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Bull Ant Antimicrobial defences: 2 – Internal • Reverse-phase HPLC• A: control haemolymph• B; challenge

haemolymph• F1, F2 inducible O-

glycosylated proline-rich antibacterial peptides

• ‘Formaecins’• Non-glycosylated

synthetic isoform had very reduced activity

• J. Biol. Chem. 273:6139-6143 (1998)

• Jim Mackintosh

F1,F2 active

against inoculum

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Summary: Bull Ant Antimicrobials:: external and internal

• Two-tier antimicrobial defence system:

1. External antiseptics from metapleural gland

2. Internal immune system with inducible peptides

• But all ant species highly eusocial – what about species at earlier stages of sociality?

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Hypothesis: Antimicrobials increase in strength with group size and level of social organisation

• EXPERIMENT:• To compare social insects that are

solitary, semi-social and eusocial• Australian bees: Amegilla,

Exoneura, Exoneurella, Trigona• Hypothesis

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Within-colony density

social

Within-colony genetic diversity

solitary

Disease Threat

Semi-social

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Sampling E. robusta– mountain ash forests

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Sampling E. nigrescens- fire induced

heathland

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E. nigrescens

0

20

40

60

80

100

120

Surface area (mm2)

Perc

en

t G

row

th

E. nigrescens

Antimicrobial ActivityNew Bioassay:

Opposing gradients of antimicrobial strength and microbial inoculum

Growth of golden

staph completely inhibited

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Antimicrobial Strength: Minimum Inhibitory Concentrations

Status Species MIC (50) MIC(100)Solitary A.cingulata 201 362Solitary A. bombif. 220 280

Semi- E. robusta 29 38Semi- E. nigresc. 15 17

Social Ex. Trident. 50 68Social T. carbon. 0.7 2.2

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ANTIMICROBIAL STRENGTH IN BEES

• density

• genetic

• diversity

• solitary semi-social eusocial

antimicrobial

POINT OF NO

RETURN?

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• Conclusions:• Group size and within-colony

relatedness inceases with increasing sociality.

• (Fungal loads were greatest in solitary species)

• Antimicrobials strong in social bees, weakest in solitaries

• Major increase in antimicrobial strength with first signs of sociality

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Antimicrobial Activity of Wasps species.

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Wasp Summary:• Social species showed significantly higher

(18x) antimicrobial activity than solitary species

• The most important variable leading to increased antimicrobial strength was increase in group size and social complexity.

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Antimicrobials in Thrips:solitary and social

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LB Control

Staph Control

Social Thrips

Wasp extract effective at 1/32nd of a wasp

equivalentSocial thrip extract effective at 50 thrip

equivalents

Social Wasps

Solitary thrip extract no effect at 180 thrip

equivalents

Lb + extract

solitary

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Concentration–growth response curves showing activity of extracts from eight thrips species against S. aureus.

Turnbull C et al. Biol. Lett. doi:10.1098/rsbl.2010.0719

©2010 by The Royal Society

Soceusoc

Semi-soc

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Next phase the only known eusocial beetle:Astroplatypus incompertus

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Antimicrobial traits and the evolution of sociality/eusociality (i)

Social evolution means increasing group size and colony complexity; manifestly increasing the need for antimicrobial defences.

Thus, the traits that enabled nascent colonies to combat microbial pathogens have been fundamental to social evolution in thrips and should be included with the other essentials.

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Antimicrobial traits and the evolution of sociality (ii) Was there a role for microbial pathogens in social evolution?

1) The first response appears to have been an increase in the strength of antimicrobial compounds.

2) Limits to this response, e.g. resource limitation or self- antibiosis might require an increase the number of individuals producing antimicrobials. This scenario embeds a role for microbial pathogens in the social evolution of thrips.

What about all the other social insect groups?

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Bioprospecting using ecological and evolutionary hypotheses

• Already big-time (NIH) (www.fic.nih.gov/programs)

• Evolutionary and Ecological Applications• J. Biological Engineering• J. Biomimicry• Hypothesis-Driven Bioprospecting

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For pharmaceuticals in general (Henkel et al. 1999,Angew. Chem. Int. Ed. 38:643)

0% 20% 40% 60% 80% 100%

molluscs (442)

insects/worms (244)

rare actinomycetes (1.915)

algae (1.276)

marine macroorganisms (2.959)

fungi (8.161)

plants (7.323)

bacteria (10.417)

BNPD total (29.432)

sugars

macrocycles

quinones

peptides

N-heterocycles

O-heterocycles

alicycles

arenes

aliphatics

others

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Sources of Drugs 1981-2002 (from Newman et al. 2003. Journal of Natural Products)

All NEW COMPOUNDS • 28% from natural product

or derivative

• 24% based on natural

product or mimic 52%

ALL ANTICANCER DRUGS• 40% from natural product

or derivative

• 21% based on natural

product or mimic 61%

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THANKS TO

• ADAM STOW• CHRISTINE TURNBULL• DAVID BRISCOE• MICHAEL GILLINGS• JIM MACINTOSH• SHANNON SMITH• HELEN DOCHERTY• RUTH BURTON• DUNCAN VEAL• PAUL DUCKETT

• KEIRA BEATTIE• DOUG BEATTIE• SAM HUSSEY • SIOBHAN DENNISION• PETER WILSON • DAVID NIPPERESS• MICHAEL SCHWARTZ• STEPHEN HOGGARD• CHRIS PALMER• TOM CHAPMAN• HOLLY CARAVAN