ESM - Monogamy in large bee societies: A stingless paradox
Electronic Supplementary Material
Electronic supplementary material for the manuscript “Monogamy in large bee societies: A
stingless paradox” by Rodolfo Jaffé, Fabiana C. Pioker-Hara, Charles F. dos Santos, Leandro R.
Santiago, Denise A. Alves, Astrid de M. P. Kleinert, Tiago M. Francoy, Maria C. Arias, and Vera L.
Imperatriz-Fonseca. Includes Material and Methods, Tables S1- S4 and References.
Material and Methods
Sampling
To collect pupae, a fireman ladder was employed to reach the nests, usually located on trees
above 6m. Using professional climbing and beekeeping equipment we then secured ourselves
to a branch at the nest level, and proceeded to drill a hole in the nest crust to open the brood
chamber. We extracted between 5 and 10 different brood combs from each nest, placed them
in Petri dishes and took them to the laboratory. Pupae were randomly collected from all combs.
All nests successfully recovered from the damage done. To collect adult workers we simply
struck the tree branches supporting the nests and waited for the bees to attack our bee suits.
All bees were collected from the suits before sampling other nests. All samples were preserved
in ethanol 95% and frozen shortly after collection. Samples were collected from three Brazilian
populations across three different biomes:
1
ESM - Monogamy in large bee societies: A stingless paradox
 Mossoró: Samples were collected during 2012 near the city of Mossoró (Rio Grande do
Norte State), at the Experimental Station of Universidade Federal Rural do Semi-Árido
(UFERSA). The region belongs to the biome Caatinga ((Por et al. 2005)).
 São Paulo: Samples were collected during 2012 in the city of São Paulo (São Paulo State), at
Universidade de São Paulo (USP). The region belongs to the biome Atlantic Forest ((Por et al.
2005)).
 Itirapina: Samples were collected between 2008 and 2010, in the Itirapina Ecological Station
and the Arruda Botelho Institute (São Paulo State). The protected area has 2,300 ha and is
one of the last reminiscents of the biome Cerrado ((Por et al. 2005)), being surrounded by
fragmented cropland and urban landscapes. Before its establishment in 1984, the Itirapina
Ecological Station consisted of grassland exposed to yearly burning. After the creation of the
Station, burning stopped allowing a process of ecological succession.
Genotyping
DNA was extracted following a Chelex protocol ((Walsh et al. 1991)) and the microsatellite
target sequences were amplified by polymerase chain reactions (PCR), using fluorescent tagged
primers ((Schuelke 2000)). PCR products were then analyzed in an ABI 3730 sequencer at
Centro de Estudos do Genoma Humano, USP. Allele sizes were checked by eye using the
software GeneMarker (Softgenetics).
2
ESM - Monogamy in large bee societies: A stingless paradox
Analyses
Pupae samples showing homozygosity at all loci were classified as males (n = 11), which in all
cases showed genotypes consistent with those of queens (Table S2). Genetic diversity measures
were computed using FSTAT (Goudet 2001), based on the genotypes of each queen and her
mate. Using the reconstructed queen genotypes we then tested for deviations from the HardyWeinberg equilibrium and calculated inbreeding coefficients using Genepop ((Rousset 2008)).
Patriline non-detection errors (the probability of failing to identify a second male because it
shares the same allele combination of the main male) were calculated for each colony following
(Foster et al. 1999). Patriline non-sampling errors (the probability of not sampling offspring
from a second male) were also calculated for each colony assuming that a putative second
patriline was represented in 50%, 25%, and 10% of offspring respectively (Foster et al. 1999).
Finally, matriline detection probability (for worker offspring produced by a daughter queen)
was calculated for each colony according to (Richards et al. 2005).
3
ESM - Monogamy in large bee societies: A stingless paradox
Table S1: Sample locations, geographic coordinates of nests, sample type, number of successfully genotyped workers (n), number of
queens detected, observed paternity, patriline non-detection error per colony (NDE), patriline non-sampling error per colony (NSE)
for patrilines represented in 50%, 25%, and 10% of offspring, and mean matriline detection probability per colony (MDP).
Colony
Location
Coordinates
Sample type
n
N. Queens
Obs. Paternity
NDE
(dn)
NSE
(50%/25%/10%)
MDP
M1
M2
M3
M4
M5
M6
S1
S2
S3
S4
S5a
I1
I2
I3
I4
I5
I6
I7
I8b
I9b
I10
I11
I12
I13
I14
I15
I16
I17
I18
I19
I20
I21
I22
I23
I24
Mossoró
Mossoró
Mossoró
Mossoró
Mossoró
Mossoró
São Paulo
São Paulo
São Paulo
São Paulo
São Paulo
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
-5.062486,-37.397988
-5.060593,-37.4053
-5.056207,-37.399795
-5.061715,-37.401695
-5.144641,-37.370356
-5.111797,-37.387265
-23.562412,-46.723047
-23.564751,-46.731136
-23.565816,-46.729781
-23.555071,-46.723796
-23.560959,-46.72072
-22.210955,-47.892226
-22.210286,-47.891253
-22.215658,-47.913921
-22.214678,-47.914734
-22.208159,-47.900689
-22.210114,-47.923092
-22.207898,-47.924355
-22.209845,-47.918986
-22.214217,-47.922285
-22.217008,-47.915655
-22.216196,-47.91967
-22.205809,-47.920056
-22.204003,-47.926106
-22.211921,-47.921966
-22.195757,-47.917852
-22.2214,-47.919875
-22.217836,-47.920829
-22.172099,-47.870702
-22.172705,-47.883932
-22.20786,-47.921931
-22.208393,-47.923434
-22.198247,-47.902812
-22.207077,-47.916283
-22.210882,-47.914966
Pupae
Pupae
Pupae
Pupae
Pupae
Pupae
Pupae
Pupae
Pupae
Pupae
Pupae
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
10
10
10
11
12
14
10
14
12
10
14
4
5
5
5
5
5
5
10
10
5
5
5
5
5
5
5
5
5
4
4
5
3
5
5
1
1
1
1
1
1
1
1
1
1
2
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
9.53X10-4
6.00X10-5
3.92X10-5
1.80X10-4
9.04X10-6
3.92X10-5
7.26X10-5
9.42X10-3
2.70X10-4
2.22X10-5
1.30X10-4
2.79X10-5
3.89X10-5
5.53X10-7
1.50X10-4
1.28X10-4
1.25X10-5
4.25X10-6
1.57X10-4
2.79X10-5
5.91X10-6
5.92x10-5
2.50X10-6
5.09X10-11
2.84X10-6
1.66X10-5
3.25X10-6
1.93X10-5
1.44X10-5
8.54X10-6
7.28X10-6
1.12X10-4
2.21X10-6
3.80X10-5
1.80X10-4
0.001/0.06/0.35
0.001/0.06/0.35
0.001/0.06/0.35
4.88x10-4/0.04/0.31
2.44x10-4/0.03/0.28
6.10x10-5/0.02/0.23
0.001/0.06/0.35
6.10x10-5/0.02/0.23
2.44x10-4/0.03/0.28
0.001/0.06/0.35
0.01/0.13/0.46
0.06/0.32/0.66
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.001/0.06/0.35
0.001/0.06/0.35
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.06/0.32/0.66
0.06/0.32/0.66
0.03/0.24/0.59
0.13/0.42/0.73
0.03/0.24/0.59
0.03/0.24/0.59
0.61
0.72
0.67
0.66
0.64
0.69
0.72
0.54
0.57
0.75
0.72
0.66
0.65
0.72
0.66
0.60
0.61
0.67
0.56
0.62
0.66
0.63
0.65
0.76
0.62
0.58
0.73
0.67
0.57
0.68
0.68
0.56
0.65
0.68
0.51
4
ESM - Monogamy in large bee societies: A stingless paradox
I25
I26
I27
I28
I29
I30
I31
I32
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
Itirapina
-22.207137,-47.903324
-22.207623,-47.904914
-22.203336,-47.90187
-22.222354,-47.908465
-22.201622,-47.924506
-22.200332,-47.920941
-22.214013,-47.921099
-22.21416,-47.917437
Adults
Adults
Adults
Adults
Adults
Adults
Adults
Adults
5
5
5
5
5
5
5
5
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
8.37X10-7
1.06X10-5
3.31X10-4
4.74X10-4
1.01X10-6
1.40X10-5
1.54X10-6
2.19X10-4
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.03/0.24/0.59
0.69
0.62
0.60
0.70
0.71
0.67
0.64
0.60
a
Genotypes consistent with the presence of two, singly mated queens. Non-detection and non-sampling errors for this colony
were calculated by averaging the estimates from both matrilines. b These colonies had two separate entrances and workers were
collected from both entrances.
5
ESM - Monogamy in large bee societies: A stingless paradox
Table S2: Genotypes from all analyzed samples (see Excel file).
Table S3: Genetic diversity per locus and population. Number of alleles (NA), expected
heterozygosity (HE) and inbreeding coefficients (FIS) are provided. FIS estimates were tested
against zero (*p<0.05; **p<0.01; ***p<0.001). (χ210 = 30.65; p < 0.001)
Population
Mossoró
Locus
NA
HE
FIS
4D
2
0.21
-0.11
2F
8
0.90
-0.13
2A
2
0.50
0.71
3G
2
0.11
N/A
Tang60
5
0.72
-0.14
Overall
3.80 ± 2.68
0.47 ± 0.14
0.06
São Paulo
4D
4
0.77
0.15
2F
5
0.71
-0.14
2A
10
0.91
0.11
3G
3
0.46
-0.05
Tang60
5
0.72
-0.54
Overall
5.40 ± 2.70
0.69 ± 0.07
-0.07
Itirapina a
4D
8
0.68
0.13
2F
9
0.73
0.15
2ª
12
0.73
-0.001
3G
5
0.58
0.33**
Tang60
8
0.61
0.25*
1B
8
0.75
0.04
1D
14
0.90
-0.02
Overall
9.14 ± 2.97
0.71 ± 0.04
0.11**
a
A significant departure from the Hardy-Weinberg equilibrium was only detected
in Itirapina population (χ210 = 30.65; p < 0.001), due to significant FIS estimates in
loci 3G and Tang60.
6
ESM - Monogamy in large bee societies: A stingless paradox
Table S4: Paternity and colony size across 58 species of social bees (only monogynous species
included). Only data from studies employing genetic markers are presented. Paternity
frequency is presented as observed paternity (Kobs) and effective paternity (me). The number of
analyzed colonies (n) and the reported colony size for each species (mean number of workers)
are also provided. Arithmetic means are given for Kobs while harmonic means are given for me.
Tribe
Species
Kobs
me
n
Colony size
References
Apini
Apis andreniformis
13.50
10.50
60
4,900
1; 2
Apini
Apis cerana
18.80
14.10
74
6,884
3; 4
Apini
Apis dorsata
54.90
44.20
140
36,630
5; 4
Apini
Apis florea
11.60
7.90
81
6,271
6; 4
Apini
Apis koschevnikovi
16.20
13.30
74
7,000
7; 8
Apini
Apis laboriosa
34.40
18.28
135
36,630
9; B. Oldroyd pers. comm.
Apini
Apis mellifera
12.00
11.60
61
19,524
10; 11; 12
Apini
Apis nigrocincta
54.00
40.30
159
6,884
Augochlorini
Augochlorella striata
1.00
1.00
24
7
Bombini
Bombus affinis
1.00
1.00
1
176
15; 11
Bombini
Bombus ardens
1.00
1.00
5
26
16; 17
Bombini
Bombus auricomus
1.00
1.00
1
35
15; 18
Bombini
Bombus bimaculatus
1.25
1.05
8
60
15; 11
Bombini
Bombus citrinus
2.50
1.76
10
50
15; B. Baer pers. comm.
Bombini
Bombus fervidus
1.00
1.00
1
88
15; 11
Bombini
Bombus griseocollis
1.00
1.00
1
46
15; 19
Bombini
Bombus honshuensis
1.00
1.00
1
200
16; 20
Bombini
Bombus hortorum
1.00
1.00
5
100
21; 11
Bombini
Bombus hypnorum
1.87
1.18
23
29
22; 21; 4
Bombini
Bombus impatiens
1.55
1.04
10
450
15; 23; 11
Bombini
Bombus lapidarius
1.00
1.00
11
200
21; 24
Bombini
Bombus lucorum
1.00
1.00
12
200
21; 11
Bombini
Bombus mixtus
4.00
3.57
5
50
15; B. Baer pers. comm.
Bombini
Bombus occidentalis
1.00
1.00
23
55
25; 26
Bombini
Bombus pascuorum
1.00
1.00
6
120
21; 24
Bombini
Bombus pratorum
1.00
1.00
5
100
21; 24
Bombini
Bombus ternarius
2.00
2.04
12
100
15; 11
Bombini
Bombus terrestris
1.00
1.00
17
350
21;24
Bombini
Bombus vagans
1.00
1.00
4
70
15; 11
Halictini
Lasioglossum malachurum
1.36
1.15
30
33
27; 28; 29
Halictini
Lasioglossum zephyrum
1.00
1.00
8
20
30; 31
Meliponini
Austroplebeia australis
1.00
1.00
2
2,000
32; 4
Meliponini
Austroplebeia symei
1.00
1.00
4
2,000
33; 4
13; B. Oldroyd pers. comm.
14
7
ESM - Monogamy in large bee societies: A stingless paradox
Meliponini
Heterotrigona hockingsi a
b
1.00
1.00
4
7,000
33; 34
1.00
1.00
4
2,000
33
1.23
2
900
Meliponini
Heterotrigona mellipes
Meliponini
Lestrimellita limao
Meliponini
Melipona beecheii
2.20
1.13
10
1,192
Meliponini
Melipona marginata
1.00
1.00
5
202
37; 34; R. Paxton unpubl.
data
38; 34
Meliponini
Melipona panamica
1.00
1.00
9
550
35; 34
Meliponini
Melipona quadrifasciata
1.00
1.00
7
350
35; 38; 34
Meliponini
Melipona scutellaris
1.00
1.00
54
992
38; 39; 34; 40
Meliponini
Nannotrigona perilampoides
1.19
7
1,125
35; 41
Meliponini
Paratrigona subnuda
1.16
11
3,750
35; 42
Meliponini
Partamona aff. cupira
0.91
12
3,390
35; 43
Meliponini
Plebeia aff. minima
1.42
5
125
35; 36
Meliponini
Plebeia droryana
1.00
1.00
2
2,960
38; 34
Meliponini
Plebeia remota
1.00
1.00
7
3,500
38; 34
Meliponini
Plebeia saiqui
1.00
1.00
4
1,500
38; 4
1.20
1.02
19
10,375
44; 34
1.00
c
35; 36
Meliponini
Scaptotrigona aff. depilis
Meliponini
Scaptotrigona barrocoloradensis
1.00
0.85
4
5,000
35; 34
Meliponini
Scaptotrigona mexicana
1.00
1.00
5
2,000
33; 45
Meliponini
Scaptotrigona pectoralis
1.00
1.00
7
4,600
33; 43
Meliponini
Schwarziana quadripunctata
1.00
1.00
22
1,650
35; 46; 34
Meliponini
Tetragona clavipes
1.00
1.00
17
7,000
35; 38; 34
1.00
1.00
5
2,750
47
1.00
1.00
4
500
1.15
7
8,500
1.00
44
92,500
Meliponini
Tetragonula carbonaria
Meliponini
Tetragonula clypearis
Meliponini
Trigona fulviventris
Meliponini
Trigona spinipes
f
e
d
1.00
33; 4
35; 43
This study; 48
Notes: a Previous Trigona hockingsi, b Previous Trigona mellipes, c Previous Scaptotrigona postica, d Previous Trigona
carbonaria, e Previous Trigona clypeari, f Previous Trigona ruficrus.
References: 1 (Oldroyd et al. 1997); 2 (Koeniger et al. 2011); 3 (Oldroyd et al. 1998); 4 (Hammond and Keller 2004);
5 (Wattanaachaiyingcharoen et al. 2003); 6 (Palmer and Oldroyd 2001); 7 (Rinderer et al. 1998); 8 (Koeniger et al.
2011); 9 (Paar et al. 2004); 10 (Estoup et al. 1994); 11 (Michener 1974); 12 (Schneider and Blyther 1988); 13
(Palmer et al. 2001); 14 (Mueller et al. 1994); 15 (Payne et al. 2003); 16 (Kokuvo et al. 2009); 17 (Katayma 1997); 18
(Katayma 1997); 19 (Cameron 1989); 20 (Ochiai and Katayama 1982); 21 (Schmid-Hempel and Schmid-Hempel
2000); 22 (Paxton et al. 2001); 23 (Cnaani et al. 2002); 24 (Westphal et al. 2006); 25 (Owen and Whidden 2013); 26
(Whittington and Winston 2003); 27 (Paxton et al. 2002); 28 (Richards et al. 1995); 29 (Soro et al. 2009); 30
(Barrows 1975); 31 (Crozier et al. 1987); 32 (Drumond et al. 2000); 33 (Palmer et al. 2002); 34 (Tóth et al. 2004); 35
(Peters et al. 1999); 36 (Roubik 1983); 37 (Paxton et al. 1999); 38 (Tóth et al. 2002b); 39 (Alves et al. 2009); 40
(Wenseleers et al. 2011); 41 (Cauich et al. 2004); 42 (Tóth et al. 2002a); 43 (Slaa et al. 2003); 44 (Paxton et al.
2003); 45 (Sánchez et al. 2004); 46 (Tóth et al. 2003); 47 (Green and Oldroyd 2002); 48 (Lindauer and Kerr 1960).
8
ESM - Monogamy in large bee societies: A stingless paradox
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