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ANTIMICROBIALS AND THE EVOLUTION OF EUSOCIALITY
Andrew Beattie
Christine Turnbull
Department of Biological Sciences
Macquarie University
Sydney, Australia
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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