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Abstract

Social Hymenoptera are characterized by a reproductive division of labour, whereby queens perform most of the reproduction and workers help to raise her offspring. A long-lasting debate is whether queens maintain this reproductive dominance by manipulating their daughter workers into remaining sterile (queen control), or if instead queens honestly signal their fertility and workers reproduce according to their own evolutionary incentives (queen signalling). Here we test these competing hypotheses using data from Vespine wasps. We show that in natural colonies of the Saxon wasp, Dolichovespula saxonica, queens emit reliable chemical cues of their true fertility and that these putative queen signals decrease as the colony develops and worker reproduction increases. Moreover, these putative pheromones of D. saxonica show significant conservation with those of Vespula vulgaris and other Vespinae, thereby arguing against fast evolution of signals as a result of a queen-worker arms race ensuing from queen control. Lastly, levels of worker reproduction in these species correspond well with their average colony kin structures, as predicted by the queen signalling hypothesis but not the queen control hypothesis. Altogether, this correlative yet comprehensive analysis provides compelling evidence that honest signalling explains levels of reproductive division of labour in social wasps. This article is protected by copyright. All rights reserved.
-3.0
-2.0
-1.0
0.0
1.0
2.0
-4.0 -2.0 0.0 2.0 4.0 6.0
PC2 (15.2%)
PC1 (42.8%)
Queens
Reproductive workers
Sterile workers
-0.2
0.0
0.2
0.4
-0.3 -0.2 -0.1 0.0 0.1 0.2 0.3 0.4
n-C31
3,7-diMeC29
3-MeC31
3-MeC29
n-C29
n-C28
A B
C D
0
1
2
3
4
5
6
01234
Ovary Score
0.0
1.0
2.0
3.0
4.0
5.0
6.0
0.4 0.5 0.6 0.7 0.8 0.9 1.0
Colony Stage
0
5
10
15
20
25
0 1 2 3 4 5 6
PC1
0
10
20
30
40
50
60
70
0 1 2 3 4 5 6
PC1
Variable Estimate p
(Intercep t) 0.50 0.88 0.384
Ovary Score 0.89 5.81
< 0.001 ** *
t
Variable Estimate p
(Intercept) Q 8.03 3.26
0.00 3 * *
Colony Stage -5.68 -1.79 0.083
Caste RW -8.47 -3.02
0.00 5 * *
Colony Stage * Caste RW 9.62 2.67
0.01 2 *
t
Variable p
(Intercep t) Q 21.96 2.63
0.013 *
PC1 -3.88 -1.78 0.084
Caste RW -16.06 -1.82 0.078
PC1 * Caste RW 6.89 2.95
0.006 **
Estimate t
Variable p
(Intercept) Q 100.66 5.44
< 0.001 ** *
PC1 -17.87 -3.71
< 0.001 ** *
Caste RW -65.97 -3.38
0.00 2 * *
PC1 * Caste RW 20.17 3.90
< 0.001 ** *
Estimate t
Peak # Component
GLMM: Q vs. SW, p < 0.01
GLMM: RW vs. SW, p < 0.01
Average Percentage
PC1 loading
PC2 loading
Q vs. SW
RW vs. SW
Q vs. SW
RW vs. SW
Q vs. W - V. crabro
Q vs. W - D. maculata
Q vs. W - V. squamosa
Q vs. W - V. maculifrons
Percentage
PCA
Log2 ratio
1n-C23 >13 >0.3 >3
2 7-,9-,11-MeC23
a5-MeC23
33-MeC23 0.0 0
b5,x -diMeC23
4n-C24
53,7-diMeC25 0 <-0.3 <-3
68-MeC24
c6-MeC24
d 4-MeC24
7,8 x-C25:1 (+isomer)
94,8-diMeC24
10 n-C25
11 7-,9-,11-,13-MeC25
12 5-MeC25
13 3-MeC25
14 5,9-diMeC25
15 n-C26
16 3,9-diMeC25
17 10-,11-,12-,13-MeC26
18 5-MeC26
19 4-MeC26
20,21 x-C27:1 (+isomer)
22 4,y-diMeC26
23 n-C27
24 9-,11-,13-MeC27
25 7-MeC27
26 5-MeC27
27 11,15-diMeC27
28 3-MeC27
29 5,11-diMeC27
30 5,y-diMeC27 + x-C28:1
31 n-C28
32 3,11-, 3,13-diMeC27
33 3,7-diMeC27
34 11-,12-,13-,14-MeC28
35 6-MeC28
36 4-MeC28
37,38 x-C29:1 (+isomer)
e4,x-diMeC28
39 n-C29
40 9-,11-,13-,15-MeC29
41 7-MeC29
42 5-MeC29
43 9,13-, 11,15-, 13,17-diMeC29
44 3-MeC29
45 5,y-diMeC29
fn-C30
46 3,9-, 3,11-, 3,13-, 3,15-diMeC29
47 3,7-diMeC29
48 12-, 13-, 14-, 15-MeC30
49 4,y-diMeC30
50 x-C31:1
51 unidentified
52 n-C31
53 13-, 15-MeC31
54 11,15-diMeC31
55 3-MeC31 + 7,13-, 7,15-diMeC31
56 5,y-diMeC31
g 13-, 15-MeC33
D. saxonica V. vulgaris Other Vespinae
PCA Log2 ratio Log2 ratio Log2 ratio
... It was amply demonstrated in A. mellifera queen's signals that change according to her mating status and quality and exerting different effects on workers and males [26,59,60]. Honest fertility signaling was also demonstrated in different ant species [61,62] as well as in social wasps [63]. The honesty of queen signals has been debated at length and the view of queen pheromones as manipulative agents was frequently challenged and mostly abandoned [5 ,8 ,9,15]. ...
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