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QUEEN SIGNALLING IN SOCIAL

Jelle S. van Zweden1,2, Cintia A. Oi1, Wim Bonckaert1, Patrizia d’Ettorre2,3 & Tom Wenseleers1

1 Laboratory of Socioecology & Social Evolution, Department of Biology, KU Leuven, Leuven, Belgium Laboratory of Socioecology 2 and Social Evolution Centre for Social Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark 3 Laboratory of Experimental and Comparative Ethology, University Paris 13, Sorbonne Paris Cité, France

Do queens of social use cuticular hydrocarbons (CHCs) to signal their fertility and regulate reproductive division of labour?

Dolichovespula saxonica vulgaris Effective queen mating frequency (# of colonies) 1.4 (35) 1.9 (17) Vespula vulgaris Worker-worker relatedness (# of colonies) 0.61 (35) 0.51 (17) Average colony size in terms of workers (# of colonies) 113 (25) 2042 (46) Queen policing present? yes no present? perhaps yes Effectiveness of policinga 0.88 0.99-1 Observed % RW in queenright colonies (# of colonies) 6.5% (22) 1.0% (6) Expected ESS % RW in queenright coloniesb 7.9% 0.0% Observed % RW in queenless colonies (# of colonies) 10.0% (19) 29.7% (10) Expected ESS % RW in queenless coloniesb 16.9% 23.4%

% RW = Percentage of reproductive workers, ESS = Evolutionary Stable Strategy Photo by (C) Josef Photo by (C) Josef a Dvorak for BWARS Dvorak for BWARS Defined as (1-Sw), where Sw is the probability that worker-laid eggs survive to adulthood relative to queen- laid eggs. b Predicted evolutionarily stable percentage of reproductive workers in queenright and queenless colonies, as described in Wenseleers et al. 2004. The degree of worker policing depends on the

0 0 PC2(7.3%)

species-average colony kin structure. PC2(15.2%)

Workers thus police according to their own fitness Sterile workers Sterile workers Reproductive workers Reproductive workers interests, not the queen’s. Queens Queens PC1 (42.8%) PC1 (67.9%)

n-C 28 n-C28

n-C29 3-MeC29 n-C27 n-C 29 3-MeC29

Dolichovespula saxonica n-C n-C31 31 3,7-diMeC29 6 6.0

PC2(7.3%) 3-MeC31?

5 5.0 3-MeC31 PC2(15.2%) 4 4.0

3 3.0

PC1 PC1 2 2.0 PC1 (42.8%) PC1 (67.9%)

1 1.0

0 0.0 0 1 2 3 4 0.4 0.5 0.6 0.7 0.8 0.9 1.0 Queen CHC profiles are separated from those of sterile workers in two species of Ovary Score Colony Stage Variable Estimate t p Variable Estimate t p Vespine wasps, and are typically characterised by linear and 3-methyl alkanes. (Intercept) 0.50 0.88 0.384 (Intercept) Q 8.03 3.26 0.003 ** Ovary Score 0.89 5.81 < 0.001 *** Colony Stage -5.68 -1.79 0.083 Caste RW -8.47 -3.02 0.005 ** Colony Stage * Caste RW 9.62 2.67 0.012 * 25 70 Dolichovespula saxonica Vespula vulgaris 60 20 50 Undeveloped ovaries Odds ratio Odds ratio

15 100% 4 100% 4

40 *** Developed ovaries

% RW % 30 10 WPM% Regressed ovaries 2 20 2 ** 5 ** * 10

0 0 1 0 1 2 3 4 5 6 0 1 2 3 4 5 6 50% 50% 1 PC1 PC1 Variable Estimate t p Variable Estimate t p 0.5 * (Intercept) Q 21.96 2.63 0.013 * (Intercept) Q 100.66 5.44 < 0.001 *** 0.5 PC1 -3.88 -1.78 0.084 PC1 -17.87 -3.71 < 0.001 *** *** ***

Caste RW -16.06 -1.82 0.078 Caste RW -65.97 -3.38 0.002 ** 0.25 *** % of workers queenless incolonies of % workers PC1 * Caste RW 6.89 2.95 0.006 ** PC1 * Caste RW 20.17 3.90 < 0.001 *** queenless incolonies of % workers Blend of n-C29, 0% 3-MeC29, n-C30, 0% 0.25 Queen CHC profile (PC1) corresponds well with ovary Control n-C31, 3-MeC31 Control n-C27 n-C28 n-C29 3-MeC29 development, colony stage, % reproductive workers, Treatment with synthetic queen-characteristic CHCs reduces worker ovary and % worker-produced males. development, so these compounds indeed function as queen .

Queen-characteristic CHCs (log2 ratio > 0)

Worker characteristic CHCs (log2 ratio < 0)

n-C22 x-C23:1 n-C23 9-,7-MeC23 5-MeC23 3-MeC23 5,y-diMeC23 n-C24 3,7-diMeC25 14-,12-, 10-MeC24 8-MeC24 6-MeC24 4-MeC24 x-C25:1 4,8-diMeC24 n-C25 13-,11-, 9-, 7-MeC25 5-MeC25 11,y-,13,y-diMeC25 3-MeC25 5,9-diMeC25 n-C26 3,9-diMeC25 (13-,12-,) 11-, 10-MeC26 5-MeC26 4-MeC26 10,y-diMeC26 3-MeC26 x-C27:1 4,y-diMeC26 n-C27 13-,11-, 9-MeC27 7-MeC27 5-MeC27 11,15-,9,13- diMeC27 7,11-,7,13-diMeC27 7,15-diMeC27 3-MeC27 5,9-,5,13-, 5,17-diMeC27 x-C28:1 n-C28 (3,13-),3,11-diMeC27 3,7-diMeC27 14-,13-, 12-, 11-, 10-MeC28 7-MeC28 6-MeC28 5-MeC28 9,y-,10,y-diMeC28 4-MeC28 3-MeC28 x-C29:1 5,y-,4,14-, 4,16-diMeC28 n-C29 15-,13-, 11-, 9-MeC29 7-MeC29 5-MeC29 13,17-,11,15-, 9,13-diMeC29 7,13-,7,y-diMeC29 3-MeC29 5,y-diMeC29 3,y-diMeC29 3,7-diMeC29 n-C30 15-,14-, 12-, 11-, 10-MeC30 6-MeC30 5-MeC30 13,17-diMeC30 4-MeC30 x-C31:1 n-C31 15-,13-, 11-, 9-MeC31 7-MeC31 5-MeC31 13,17-,11,15-diMeC31 3-MeC31 5,y-diMeC31 3,11-diMeC31 n-C32 16-,15-, 14-MeC32 8-MeC32 7-MeC32 12,16-diMeC32 8,14-diMeC32 C33:1 n-C33 17-,15-, 13-, 11-, 9-MeC33 7-MeC33 5-MeC33 13,17-diMeC33 7,15-diMeC33 5,15-diMeC33 13-,12-, 11-MeC34 6,y-diMeC34 n-C35 17-,15-, 13-, 11-MeC35 7-MeC35 5-MeC35 13,17-,11,15-diMeC35 7,15-diMeC35 5,15-,5,17-diMeC35 19-,17-, 15-, 13-MeC37 dominula Polistes satan Vespa crabro Dolichovespula maculata Dolichovespula media Dolichovespula sylvestris Dolichovespula saxonica Vespula squamosa Vespula maculifrons Vespula vulgaris

Queen-characteristic CHCs are by and large conserved between social Vespid species, consistent with slow rates of evolution and thus arguing against queen-worker arms races over reproduction.

These data are consistent with the hypothesis that queens of social Vespidae reliably signal their fertility and workers respond according to their own fitness interests. The data argue against queen control over reproduction and queen-worker arms races.

References: Oi et al, unpublished results; van Zweden et al. 2014, Evolution 68: 976-986; Van Oystaeyen et al. 2014, Science 287: 287-290; Bonckaert et al. 2011, Mol Ecol 20: 3455-3468; Wenseleers & Ratnieks 2006, Nature 444: 50; Wenseleers et al. 2004, J Evol Biol 17: 1035-1047; Butts et al. 1991, Comp Biochem Physiol B: 99: 87-91