Defending the fortress: hostparasite interactions in social insects

1
Defending the fortress host-parasite
interactions in social insects

• William Hughes

• Outline of lecture
• Group-living and disease
• Parasites of social insects
• Social insect defences

2
Group-living and disease

• Group-living can have benefits.....
• E.g.1 predator confusion
• E.g.2 conserving heat
• E.g.3 cooperation
• .....but can also have costs
• E.g.1 interference
• E.g.2 parasites

3
Group-living and disease
The mass action principle
I
SPv

Number of new infections per unit time (I)
Density of susceptible hosts (S)
Density of infectious parasites (P)
Transmission parameter (v)

x
x

• Group-living involves a higher S
• So group-living can mean more transmission

4
Group-living and disease

• Transmission and virulence are related
• Vertical transmission lower virulence
• Horizontal transmission higher virulence
• Need for mobile hosts lower virulence
• Less need for mobile hosts higher virulence
• E.g.1 vectors
• E.g.2 high density of hosts

5
Group-living and disease

• Group genetic diversity
• Social insect colonies
• normally have low genetic diversity which means
• all group members may be susceptible
• parasites may transmit more readily
• parasites can adapt within the group more easily

x
6
Group-living and disease

• Summary
• Social insects may be particularly vulnerable to
  parasites because
• Higher density of potential hosts
• Higher rate of transmission
• Higher virulence can evolve
• Low genetic diversity
• All group member may be susceptible
• Easier for parasite to transmit and adapt within
  group
• Constant environment
• Less need for parasite to have durable
  transmission stages
• More fragile parasites can persist

7
Parasites of social insects

• Microparasites
• Viruses
• Bacteria
• Fungi
• Protozoa

• Macroparasites
• Nematode worms
• Helminth worms
• Mites
• Parasitoids
• Social parasites

8
Parasites of social insects host biology
NB General host biology only. There are always
exceptions
9
Parasites of social insects

• Social insects suffer from a range of parasites
• Biological details make different host taxa more
  or less at risk from the different types of
  parasite
• Knowledge is incomplete, particularly for less
  virulent parasites
• However, it appears that in general social
  insects may not suffer as much from parasites as
  expected

10
Social insect defences

• Stages
• Exposure
• Individual defences
• Group defences I
• Group defences II

Boomsma et al. 2005 in Insect Evolutionary
Ecology by Fellowes, Holloway and Rolff
11
Social insect defences exposure

• Group-living may involve high intragroup
  transmission
• But it may also involve low intergroup
  transmission

uninfected
infected
Wilson et al. 2003 J An Ecol 72133-143
12
Social insect defences individual-level

• Recognition and avoidance
• Immune response
• Cellular (phagocytosis, encapsulation)
• Humoral (antibacterial peptides etc.)
• Oral filters, e.g. infrabuccal filter in ants
• Self-grooming
• Antibiotic excretions

13
Social insect defences group-level I

• Recognition and exclusion
• Transfer of antibiotic secretions
• Allogrooming
• Can make individuals in a group more resistant
  than when alone

14
Social insect defences - refs

• Hughes et al. 2002 Proc Roy Soc Lond
  2691811-1819
• Poulsen et al. 2002 Behav Ecol Soc 52151-157
• Wilson et al. 2003 J An Ecol 72133-143
• Boomsma et al. 2005 in Insect Evolutionary
  Ecology by Fellowes, Holloway and Rolff

15
Social insect defences group-level II

• Waste management
• Organisation of work
• Division of labour
• Task partitioning
• Increased genetic diversity

16
Social insect defences waste management

• Societies generate waste
• Dead individuals
• Sewage
• Food rubbish

• Waste can be hazardous to colony members
• Waste can also be hazardous to crops and food
  stores

17
Social insect defences waste management - refs

• Bot ANM, Currie CR, Hart AG and Boomsma JJ 2001.
  Ethology, Ecology and Evolution, 3 225-237
• Hart, A. G. and F. L. W. Ratnieks. 2001.
  Behavioral Ecology and Sociobiology 49387-392.
• Hart AG and Ratnieks FLW 2002. Behavioral
  Ecology, 13 224-231
• Hart AG, Bot ANM and Brown MJF 2002.
  Naturwissenschaften 89275-277

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Social insect defences - organisation of work

• Division of labour
• Only certain individuals deal with waste
• These may be kept away from the rest of the
  colony
• Those individuals at the front-line may be better
  defended
• Task partitioning
• Task of waste removal may be partitioned to
  minimise contamination
• Waste may be transferred indirectly to minimise
  contamination

19
Social insect defences - organisation of work -
refs

• Ratnieks, F. L. W., and C. Anderson. 1999.
  Insectes Sociaux 4695-108.
• Hart, A. G. and F. L. W. Ratnieks. 2001. Animal
  Behaviour 62227-234
• Hart, A. G. and F. L. W. Ratnieks. 2001.
  Behavioral Ecology and Sociobiology 49387-392.

20
Social insect defences - genetic diversity

• Genetic diversity of workers within the colony
  may be increased by polygny or polyandry
• Genotypes may differ in resistance to parasites

21
Herd immunity
Social insect defences - genetic diversity
susceptible
resistant
infected
Anderson May 1985 Nature 318323-329
22
Social insect defences - genetic diversity

• Summary
• Increased by polyandry and polygyny
• May be beneficial to group due to
• Herd immunity
• More average infection/survival
• Transfer of resistance
• Harder for parasite to adapt to

23
Social insect defences - genetic diversity - refs

• Anderson May 1985 Nature 318323-329
• Baer et al. 1999 Nature 397151-154
• Hughes Boomsma 2004 Evolution 581251-1260
• Tarpy 2002 Proc. Roy Soc Lond 27099-103
• Hughes Boomsma 2006 J Evol Biol 19132-143
• Seeley Tarpy 2007 Proc. R. Soc. Lond B
  27467-72

24
Conclusions

• Group-living should be associated with increased
  disease pressure
• Social insects do suffer from a range of
  parasites
• Biological details mean different hosts are more
  or less susceptible to different parasites
• Social insects have evolved a suite of
  sophisticated defences against parasites
• As a result, they apparently do not suffer from
  parasites as much as we might expect

w.o.h.hughes_at_leeds.ac.uk