Rapid decision-making with side-specific perceptual discrimination in ants.
BACKGROUND
Timely decision making is crucial for survival and reproduction. Organisms often face a speed-accuracy trade-off, as fully informed, accurate decisions require time-consuming gathering and treatment of information. Optimal strategies for decision-making should therefore vary depending on the context. In mammals, there is mounting evidence that multiple systems of perceptual discrimination based on different neural circuits emphasize either fast responses or accurate treatment of stimuli depending on the context.


RESULTS
We used the ant Camponotus aethiops to test the prediction that fast information processing achieved through direct neural pathways should be favored in situations where quick reactions are adaptive. Social insects discriminate readily between harmless group-members and dangerous strangers using easily accessible cuticular hydrocarbons as nestmate recognition cues. We show that i) tethered ants display rapid aggressive reactions upon presentation of non-nestmate odor (120 to 160 ms); ii) ants' aggressiveness towards non-nestmates can be specifically reduced by exposure to non-nestmate odor only, showing that social interactions are not required to alter responses towards non-nestmates; iii) decision-making by ants does not require information transfer between brain hemispheres, but relies on side-specific decision rules.


CONCLUSIONS
Our results strongly suggest that first-order olfactory processing centers (up to the antennal lobes) are likely to play a key role in ant nestmate recognition. We hypothesize that the coarse level of discrimination achieved in the antennal lobes early in odor processing provides enough information to determine appropriate behavioral responses towards non-nestmates. This asks for a reappraisal of the mechanisms underlying social recognition in insects.
Stroeymeyt
Nathalie
N
Department of Biology, Centre for Social Evolution, University of Copenhagen, Copenhagen, Denmark. Nathalie.Stroeymeyt@bristol.ac.uk
Guerrieri
Fernando J
FJ
van Zweden
Jelle S
JS
d'Ettorre
Patrizia
P
D000818:Animals; D001000:Ants / Q000187:drug effects / Q000378:metabolism / Q000502:physiology*; D003463:Cues; D003657:Decision Making / Q000187:drug effects / Q000502:physiology*; D004192:Discrimination, Psychological / Q000187:drug effects / Q000502:physiology*; D007839:Functional Laterality / Q000502:physiology*; D006838:Hydrocarbons / Q000494:pharmacology; D009425:Nesting Behavior; D009812:Odorants; D021641:Recognition, Psychology / Q000187:drug effects; D013997:Time Factors
D006838:Hydrocarbons
Annu Rev Entomol. 1989;34:477-501
2648971
Proc Biol Sci. 2008 Oct 22;275(1649):2353-61
18611852
Cell Tissue Res. 1988 Nov;254(2):255-81
3197087
Learn Mem. 2002 Sep-Oct;9(5):337-48
12359841
Proc Biol Sci. 2009 Jul 7;276(1666):2461-8
19364750
Curr Biol. 2005 Dec 6;15(23):2170-4
16332544
Science. 1999 Oct 22;286(5440):723-8
10531051
Nature. 1998 Jun 4;393(6684):467-70
9624001
J Exp Biol. 2008 Apr;211(Pt 7):1109-13
18344485
Brain Res. 1994 Jul 18;651(1-2):317-28
7922581
Behav Res Methods Instrum Comput. 2000 Aug;32(3):446-9
11029818
Chem Senses. 2005 May;30(4):327-35
15788713
J R Soc Interface. 2006 Apr 22;3(7):243-54
16849234
Front Comput Neurosci. 2009 Jan 15;2:9
19221584
Curr Opin Neurobiol. 2003 Dec;13(6):726-35
14662375
Learn Mem. 2001 Sep-Oct;8(5):286-94
11584076
J Insect Physiol. 2009 Feb;55(2):158-63
19041322
Science. 2005 Jul 8;309(5732):311-4
15947139
Vision Res. 2008 Jun;48(12):1345-73
18452967
J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2007 Sep;193(9):993-1000
17639411
Proc Biol Sci. 2004 Jul 7;271(1546):1427-34
15306343
Proc Natl Acad Sci U S A. 2001 Mar 27;98(7):3898-903
11259668
Science. 1982 Jul 16;217(4556):220-5
7089556
Proc Biol Sci. 2007 Jun 7;274(1616):1421-8
17389223
Neuron. 2004 Dec 2;44(5):865-76
15572116
Neuron. 2006 Aug 3;51(3):351-8
16880129
Nat Rev Neurosci. 2006 Jun;7(6):485-91
16715056
J Neurosci. 2010 Mar 17;30(11):3896-903
20237260
Annu Rev Entomol. 2005;50:371-93
15355247
Chem Senses. 2005 Jul;30(6):477-89
15917370
Trends Ecol Evol. 2009 Jul;24(7):400-7
19409649
J Chem Ecol. 2009 Aug;35(8):913-21
19629598
Annu Rev Entomol. 2001;46:573-99
11112180
Nat Neurosci. 2003 Jun;6(6):624-31
12740580
J R Soc Interface. 2009 Nov 6;6(40):1065-74
19324679
Nature. 2006 Nov 16;444(7117):295-301
17108953
Behav Neurosci. 2009 Feb;123(1):36-43
19170428
J Neurophysiol. 1992 Mar;67(3):588-98
1578245
Nature. 2003 May 1;423(6935):32
12721617
Behav Brain Res. 2003 Oct 17;145(1-2):135-43
14529812
Nature. 2009 Jan 15;457(7227):262-3
19148082
Nat Neurosci. 2003 Nov;6(11):1224-9
14566341
Chem Senses. 2003 Nov;28(9):781-9
14654446
J Neurosci. 2001 Aug 15;21(16):6274-82
11487650
Cell Mol Life Sci. 2009 Jul;66(13):2135-50
19294334