ANTIMICROBIALS AND THE
EVOLUTION OF EUSOCIALITY
Andrew Beattie
Christine Turnbull
Department of Biological Sciences
Macquarie University
Sydney, Australia
andrew.beattie@mq.edu.au
1
The major social insects
Ants (© Ron Oldfield)
Social wasps
©Micropolitan.org
Social bees
©2008 Peter O
www.aussiebee.com.au
Termites
www.evergreenpest.com.au
2
Criteria for Eusociality
1. Cooperative brood care
2. Reproductive division of labour; castes
3. Overlap between at least two
generations; offspring assist parents
4. Is there another one?
3
THIS TALK
•
•
•
•
•
Bull ants
Bees
Wasps
Thrips
(Bioprospecting)
4
5
Bull Ants have two defences against
antimicrobial attack
1. EXTERNAL
• Paired metapleural
glands
• Strong antiseptic
6
Extracting antimicrobial metapleural secretions
7
Metapleural secretion activity against
microorganisms
Yeasts (fungi):strong
Gram + bacteria:mixed
Gram –ve: strong
8
Bull Ant Antimicrobial defences:
2 – Internal
•
•
•
•
•
•
•
•
Reverse-phase HPLC
A: control haemolymph
B; challenge haemolymph
F1, F2 inducible Oglycosylated proline-rich
antibacterial peptides
‘Formaecins’
Non-glycosylated
synthetic isoform had very
reduced activity
J. Biol. Chem. 273:61396143 (1998)
Jim Mackintosh
F1,F2
active
against
inoculum
9
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?
10
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
11
Within-colony
density
Disease
Threat
Within-colony
genetic
diversity
solitary
Semi-social
social
12
Sampling E. robusta–
mountain ash forests
13
Sampling E. nigrescensfire induced
heathland
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E. nigrescens
Antimicrobial
Activity
120
100
80
New Bioassay:
60
40
20
0
1.
80
2.
40
3.
21
4.
27
5.
70
7.
60
10
.1
3
13
.5
1
18
.0
1
24
.0
1
32
.0
1
42
.6
9
Percent Growth
E. nigrescens
2
Surface area (mm )
Opposing
gradients of
antimicrobial
strength and
microbial
inoculum
Growth of golden
staph completely
inhibited
15
Antimicrobial Strength: Minimum Inhibitory
Concentrations
Status Species
Solitary A.cingulata
Solitary A. bombif.
MIC (50)
201
220
MIC(100)
362
280
SemiSemi-
E. robusta
E. nigresc.
29
15
38
17
Social
Social
Ex. Trident.
T. carbon.
50
0.7
68
2.2
16
•
ANTIMICROBIAL STRENGTH IN BEES
POINT OF
NO
RETURN?
density
•
•
•
genetic
diversity
solitary
semi-social
eusocial
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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.
20
Antimicrobials in Thrips:
solitary
and social
21
LB Control
Lb +
extract
Social
Thrips
Social
Wasps
solitary
Staph Control
Solitary thrip extract no
effect at 180 thrip
equivalents
Wasp extract effective
at 1/32nd of a wasp
equivalent
Social thrip extract
effective at 50 thrip
equivalents
22
Concentration–growth response curves showing activity of extracts from eight thrips species
against S. aureus.
Soc
eusoc
Semi
-soc
Turnbull C et al. Biol. Lett. doi:10.1098/rsbl.2010.0719
23
©2010 by The Royal Society
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.
25
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 selfantibiosis 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?
26
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
27
For pharmaceuticals in general (Henkel et al.
1999,Angew. Chem. Int. Ed. 38:643)
BNPD total (29.432)
bacteria (10.417)
sugars
macrocycles
plants (7.323)
quinones
fungi (8.161)
peptides
N-heterocycles
marine macroorganisms (2.959)
O-heterocycles
algae (1.276)
alicycles
arenes
rare actinomycetes (1.915)
aliphatics
others
insects/worms (244)
molluscs (442)
0%
20%
40%
60%
80%
100%
28
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%
29
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THANKS TO
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ADAM STOW
CHRISTINE TURNBULL
DAVID BRISCOE
MICHAEL GILLINGS
JIM MACINTOSH
SHANNON SMITH
HELEN DOCHERTY
RUTH BURTON
DUNCAN VEAL
PAUL DUCKETT
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KEIRA BEATTIE
DOUG BEATTIE
SAM HUSSEY
SIOBHAN DENNISION
PETER WILSON
DAVID NIPPERESS
MICHAEL SCHWARTZ
STEPHEN HOGGARD
CHRIS PALMER
TOM CHAPMAN
HOLLY CARAVAN
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