Insectes Sociaux, Paris

9 Masson, Paris, 1987

1987, V o l u m e 34, n ~ 4, pp. 298-307

MATERNAL AND PRE ECLOSIONAL FACTORS AFFECTING ALARM BEHAVIOUR IN ADULT HONEY BEES (APIS MELLIFERA L.) R.F.A. MORITZ (1), E.E. SOUTHWICK (1) and J.R. HARBO (2) (1) Department of Biological Sciences, State University of New York, Brockport N Y 14420, USA. (2) Bee Breeding and Stock Center Laboratory, USDA, ARS, 1157 Ben Hur Rd, Baton Rouge LA 70820, USA. Requ le 4 d4cembre 1986

Accept6 le 25 aofit 1987

SUMMARY The inheritance of a group character, the alarm behaviour of honey bee workers

(Apis rnellifera L.), was analyzed using a metabolic bio-assay. In a diaUel test cross of preselected queens and drones, genetic variance and maternal effects on this behaviour were estimated. Crossfostering experiments showed that the hive environment during larval and pupal development has only minor effects on alarm behaviour.

ZUSAMMENFASSUNG Maternale und pr~imaginale Kolonieeffekte auf Alarmverhalten yon Honigbienen (Apis mellifera L.) Die Vererbung eines Gruppenmerkmales, der Alarmierungsreaktion yon Arbeiterinnen (Apis mellifera L.) wurde in einem quantitativen Stoffwechselte~t fiberpriift. In einer diallelen Testkreuzung von selektierten KSniginnen und Drohnen konnten genetische Varianzkomponenten sowie maternale Effekte geschStzt werden. Experimente, in denen Eier yon fremden PflegevSlkern zu Imagines aufgezogen wurden, zeigten, dass die Stockumwelt w~ihrend der Larval -und Pupalentwicklung keinen Einfluss auf das sp~itere Alarmverhalten der Arbeiterinnen nimmt.

INTRODUCTION In highly social organisms and especially in eusocial insects, b e h a v i o u r a l p a t t e r n s f r e q u e n t l y r e s u l t f r o m s o c i a l i n t e r a c t i o n s b e t w e e n g e n e t i c a l l y diff e r e n t , b u t r e l a t e d , m e m b e r s of t h e s o c i e t y . A t y p i c a l e x a m p l e f o r s u c h a

R.F.A. M O R I T Z , E.E. S O U T H W I C K and ].R. H A R B O

299

s o c i a l g r o u p b e h a v i o u r is t h e a l a r m b e h a v i o u r i n h o n e y b e e s (Apis mellifera L.). G r o u p s o f h o n e y b e e s r e s p o n d t o a l a r m p h e r o m o n e s w i t h a t y p i c a l b e h a v i o u r a l p a t t e r n (MASCHWITZ, 1964). T h e s o c i a l c o n t e x t o f t h e g r o u p , h o w e v e r , is a n a b s o l u t e n e c c e s s i t y f o r t h i s b e h a v i o u r a n d i s o l a t e d i n d i v i d u a l b e e s d o n o t s h o w t h e t y p i c a l r e a c t i o n t o a l a r m p h e r o m o n e s (SOUTHWICKa n d MORITZ, 1985). S u c h g r o u p e f f e c t s a r e r e p e a t e d l y r e p o r t e d f o r e u s o c i a l ins e c t s (CHAUVIn, 1981; GORDON, 1982; SITBON, 1967, 1971) a n d t h e y a r e o f major importance for the regulation of social mechanisms within colonies. T h e q u a n t i t a t i v e g e n e t i c a n a l y s i s o~ g r o u p c h a r a c t e r s is m o r e c o m p l e x than analyzing behavioural characters of individuals. The genetic structure of a group requires redefinitions of the basic estimators of quantitative g e n e t i c s (MoRITZ, 1986). I n h o n e y b e e s t h e m o n o g y n y o f c o l o n i e s a n d t h e p o l y a n d r y o f q u e e n s h a v e t o b e c o n s i d e r e d w h e n e s t i m a t e s o f g e n e t i c var i a n c e s o f g r o u p c h a r a c t e r s a r e m a d e (LAIDLAW a n d PAGE, 1984; MORITZ, 1986b). B e s i d e s a d d i t i v e a n d n o n - a d d i t i v e g e n e e f f e c t s , a l s o a d d i t i v e a n d non-additive genotype interactions are important factors in the expression of a certain group phenotype. Maternal effects are thought to play a minor r o l e in i n s e c t s , s i n c e t h e e m b r y o n a l e n v i r o n m e n t is less d e p e n d e n t o n t h e m o t h e r t h a n e.g. i n m a m m a l s . N e v e r t h e l e s s , m a t e r n a l e f f e c t s o n i n s e c t s h a v e b e e n r e p e a t e d l y r e p o r t e d , a n d w e r e r e c e n t l y r e v i e w e d b y SANDER (1984). T h e i n t r a - c o l o n y e n v i r o n m e n t , w h i c h is l i k e l y to b e d e p e n d e n t o n t h e genotype of the workers, also may have effects on the developing larvae. The present study shows how maternal effects and colony environment p r i o r to e c l o s i o n c a n d e t e r m i n e a s o c i a l g r o u p b e h a v i a u r .

MATERIALS

AND METHODS

The defensive behaviour of 30 equal sized honey bee colonies (A. mellifera L.) was tested in the field using a simple target bio-assay similar to STORT (1974) and COLLINS et aL (1982). The colonies were placed on three locations with similar foraging conditions in the vicinity of the USDA Bee Genetics and Physiology Laboratory in Baton Rouge, Louisiana. In order to avoid effects by neighboring colonies, only colonies more than 15 m apart were tested. The testing sequence was random for every test series on each site. During the period of testing the colonies (early April, 1985), environmental conditions were very constant in Louisiana (ca 20~ C, sunny). Tests were always performed around 1200 h local time to keep effects of radiation and basic colony activity similar on all test days. The lid of each hive was opened and a piece of filter paper, soaked with lml diluted Isopentyl acetate (IPA, 1% in paraffin oil), a major compound of the alarm pheromone, was placed in the center of the top of the colony. Simultaneously a 5 cm • 5 cm red suede leather target was moved back and forth 1 cm above the hive for 15 sec. This test was repeated after two days and the average number of stings per target was used to rank the colonies corresponding to their behaviour. Six colonies, 2 with high, 2 with medium and 2 with low defensive behaviour, were selected from the test population to produce the queens and drones for a diallel testcross system as shown in table I. Thirty-six queens were inseminated with semen from

ALARM B E H A V I O U R I N H O N E Y B E E S

300

T a b l e I. -- I n s e m i n a t i o n p e d i g r e e o f t h e e x p e r i m e n t a l colonie. A n i n c o m p l e t e diallel s e t w a s u s e d in o r d e r to a v i o d i n b r e e d i n g . L = l o w d e f e n s i v e b e h a v i o u r , M = m e d i u m defensive behaviour, H = high defensive behaviour. Two colonies per behavioural t y p e ( s u b s c r i p t 1 a n d 2) w e r e s e l e c t e d . A r e p l i c a t e o f e a c h c r o s s w a s m a d e , g i v i n g a t o t a l o f 36 c o l o n i e s i n v o l v e d i n t h e e x p e r i m e n t . T a b e l l e I. -- B e s a m u n g s s c h e m a der experimentellen KSniginnen. Ein inkomplettes dialleles K r e u z u n g s s y s t e m w u r d e u n t e r V e r m e i d u n g y o n I n z u c h t a n g e s e t z t . L = s c h w a c h e s , M = m i t t l e r e s , H = s t a r k e s V e r t e i d i g u n g s v e r h a l t e n . J e w e i l s zwei K o l o n i e n ( S u b s k r i p t 1 u n d 2) p r o V e r h a l t e n s t y p u s w u r d e n a u s d e r o r i g i n a l e n P o p u l a t i o n s e l e k t i e r t . V o n j e d e r K r e u z u n g w u r d e eine W i e d e r h o l u n g e r s t e l l t , so da~ i n s g e s a m t 36 V S l k e r z u r V e r f f i g u n g s t a n d e n . Queen

Drone

mother

mother

L1

L2

M I

M 2

L1

--

I~

L2L 1

M1

--

,~qI2

M2L 1

H:

H2

H I

H 2

L:L 2

--

--

L2M 1

LxM 2

--

L:H 2

--

L2H 1

--

M1L 2

--

M1M 2

--

--

M2M 1

--

M2H 1

--

--

H:L 2

--

H:M 2

--

H:H 2

H2L:

--

H2M:

--

H2H 1

--

MIH 2

a l a r g e h o m o g e n e o u s l y m i x e d s e m e n p o o l o f m o r e t h a n 100 d r o n e s of t h e c o r r e s p o n d i n g d r o n e m o t h e r (sire q u e e n ) (MORITZ, 1983). T h i s a l l o w e d f o r a m o r e a c c u r a t e e s t i m a t e of g e n e t i c v a r i a n c e , s i n c e e a c h q u e e n in a ' s i r e g r o u p w a s i n s e m i n a t e d w i t h g e n e t i c a l l y i d e n t i c a l s e m e n . T h e q u e e n s w e r e i n t r o d u c e d i n t o e q u a l size c o l o n i e s (10 f r a m e s ) . S e a l e d w o r k e r b r o o d o f t h e e x p e r i m e n t a l q u e e n s w a s p l a c e d in a n i n c u b a t o r (35 ~ C, 65 % R H ) . F r e s h l y e m e r g e d w o r k e r s ( < 12 h) w e r e c a g e d i n g r o u p s o f 40 a n d k e p t a t 28 ~ C, 65 % R H i n c o n s t a n t d a r k ( h o n e y a n d p o l l e n ad l i b i t u m ) . F o u r d a y s a f t e r e m e r g e n c e t h e r e a c t i o n o f t h e g r o u p s to I P A w a s t e s t e d i n a m e t a b o l i c b i o - a s s a y as d e s c r i b e d p r e v i o u s l y (SOUTHW:CK a n d MORITZ, 1985; MORITZ et al., 1985). T h e g r o u p s r e a c t w i t h a t y p i c a l i n c r e a s e i n t h e i r m e t a b o l i c a c t i v i t y w h e n e x p o s e d to IPA. T h i s is m e a s u r e d b y t h e i n c r e a s e i n o x y g e n c o n s u m p t i o n p e r bee, AVO 2 [ u l / b e e / m i n ] . Five g r o u p s w e r e t e s t e d f r o m e a c h t e s t c o l o n y , w h i c h t o t a l s n = 180 m e a s u r e m e n t s . I n o r d e r to d e m o n s t r a t e p o s s i b l e e f f e c t s o f c o m m o n h i v e e n v i r o n m e n t , w e p e r f o r m e d a c r o s s f o s t e r i n g d e s i g n a s s u g g e s t e d b y (RISKA et al., 1985). B r o o d c o m b s w e r e s w i t c h e d between colonies and eggs and larvae from two low reactive colonies were reared by h i g h l y r e a c t i v e b e e s a n d vice v e r s a . A f t e r t h e b r o o d cells w e r e c a p p e d (8 d a y s to ensure that no offspring of the foster queen was tested) and pupation had started, the brood was placed in an incubator until emergence of the imaginals. These were then tested using the same method as described above.

RESULTS

Figure 1 shows the distribution of the n u m b e r of stings p e r test per colony in the field test p r i o r to selection. The field test was repeated on t w o different days, and we found a significant two r a n k correlation of the

R.F.A. MORITZ, E.E. SOUTHWICK and J.R. HARBO

301

30

2O

g I0

0

,V |

I0

I

I I

I

3O

I

5O

!

I

70

i

J

I

90

number of stings Fig. 1. - - Frequency in % (y-axis) of number of stings (x-axis) per target per colony (field test) m the tested population. At the average 48.2 - 9.1 stings were counted per target in a 15 sec test. Abb. 1. - - H~iufigkeit in % (y-Achse) der Anzahl Stiche pro Zielobjekt (x-Achse) und Kolonie im Feldtest. Im Mittel wurden 48.2 _--4-9.1 Stiche pro Zielobjekt im 10 sec Test erhalten.

n u m b e r o f s t i n g s p e r t a r g e t b e t w e e n t h e t e s t d a y s (rs = 0.48; p < 0.01). T h e m e a n n u m b e r o f s t i n g s in t h e t a r g e t w a s 52.4 - 9.1. T h e s e l e c t e d colon i e s s h o w e d 77.3 - 12.1, 73.0 m 11.0 (H1, H2, h i g h ) , 51.3 - 8.3, 46.3 -+ 8.5 (M1, M2, m e d i u m ) , a n d 27.4 -+ 5.1, 18.2 - 6.2 (L1, I_~., low) s t i n g s p e r t a r g e t per test on the average. Figure 2 s h o w s t h e r e g r e s s i o n o f t h e m e t a b o l i c r e a c t i o n o f t e s t g r o u p s o f o f f s p r i n g c o l o n i e s o n t h e m e a n n u m b e r of s t i n g s i n t h e f i e l d t e s t o f t h e p a r e n t s . T h e r e g r e s s i o n c o e f f i c i e n t b = 0.25 (SD = 0.024) is s i g n i f i c a n t l y l a r g e r t h a n z e r o (t = 10.25, p < 0.01) a n d 76 % o f t h e t o t a l v a r i a n c e c a n b e e x p l a i n e d b y r e g r e s s i o n (r2 = 0.76). T h e r e a l s o is a d i f f e r e n c e b e t w e e n t h e reciprocal crosses (filled circles predominently above and open circles below t h e r e g r e s s i o n line), w h i c h is a n i n d i c a t i o n f o r p o s s i b l e m a t e r n a l e f f e c t s . T h e a c t u a l a n a l y s i s o f m a t e r n a l e f f e c t s w a s m a d e i n a sib a n a l y s i s a s

ALARM BEHAVIOUR IN HONEY BEES

302

Hj H2 JJI/ bee /min 20 4 " S " ~ I'~

A

L~ H l

t-o~ I,.

r of)

9 j*

LI.M!

0

000 0 ,4--

o o

I0

L2M2 s"

o

9~

;o 0

M2H2

0 MI M2 0 L2H?_

0 o

,,I,-,

r

E

4 S

LI

,

!

L?.

O. I0

I

30

!

I

50

I

i .......

I

70

number of stings (parents mean) Fig. 2. - - Regression of average metabolic reactions of offspring test groups (y-axis) on the n u m b e r of stings of the p a r e n t colonies (x-axis) in the field (arithmetic m e a n of b o t h parents), 9 = queen b r e e d e r colony has a higher score in the field test t h a n d r o n e m o t h e r colony, O = reciprocal m a t i n g type, Abb. 2. - - Regression tier Stoffwechselreaktion der T e s t g r u p p e n (y-Achse) auf die mittlere Anzahl Stiche d e r Elternkolonien im Freilandtest (x-Achse). 6 = KSniginnenmuttervolk hat ein stiirkeres Verteidigungsverhalten als Vatervolk. O = reziproke Kreuzung.

s h o w n in table II. The average increase in oxygen c o n s u m p t i o n a f t e r IPA application in o u r b/o-assay was 11.05 -+ 0.41 ~lO~/bee/min. Genetic variances w e r e estimated using the intraclass correlation according to the p r o c e d u r e suggested by OLDROYD and MORAN (1983). Maternal effects w e r e analysed using the model of DICKERSON (1962) and WILLUAM (1964). S t a n d a r d e r r o r s of the estimate for the intraclass correlations w e r e calculated according to e q u a t i o n 13.2.6 of SNEDECOR and COCHRAN (1980). The relationship o f test groups with c o m m o n dams, m a y be subject to estimation e r r o r s because of the u n k n o w n degree of polyandry in natural matings of the b r e e d e r queens. Assuming that 10 drones mate with one queen at the average (KoENIGER,

R.F.A. MORITZ, E.E. SOUTHWICK and J.R. HARBO

303

1986) we o b t a i n a relationship of r = 0.263. The relationship a m o n g groups w i t h c o m m o n sires is 0.5. Using FALCONER'S (1981) for the estimation of the heritability : h2 = t/r 9vhere : t = intraclass correlation r -- probability for genes identical by descent in two test groups within sires o r dams respectively the estimate for h 2 in the n a r r o w sense (selectability) f r o m the sire variance c o m p o n e n t is h 2 = 0.36 -- 0.14 and the estimate for the m a t e r n a l c o m p o n e n t f r o m the d a m variance is m = 0.65 - 0.62. I n t e r a c t i o n s due to dominance effects or interactions between genotypes within the test groups are est i m a t e d f r o m the sire x d a m variance c o m p o n e n t with d = 0.43 __ 0.37. The o t h e r variance c o m p o n e n t s a p p e a r e d not to be significantly larger t h a n zero and t h e r e f o r e are not f u r t h e r analysed. The crossfortering experiment s h o w e d no significant effect of hive e n v i r o n m e n t on a l a r m behaviour (table III). The metabolic reaction of the test groups correlated to the genotype of the genetic m o t h e r b u t not to the genotype of the foster colony. There is also no effect of the length of devel o p m e n t time in the foster colony. Regardless of h o w long the larvae were i n t r o d u c e d before the capping of the cell (0 to 8 days), the average test group reaction did not change significantly over time of foster b r o o d care. Regression coefficients for group reaction on foster d u r a t i o n were f o u n d to be n o t significantly different f r o m zero.

DISCUSSION The genetic analysis of the a l a r m b e h a v i o u r of h o n e y bess in this study, shows that genetic factors indeed have considerable i m p a c t for this character. The estimate for the total genetic variance, including additive, d o m i n a n c e a n d m a t e r n a l components, fits well to a previous study in w h i c h the coefficient of genetic d e t e r m i n a t i o n for this c h a r a c t e r was estimated in African a n d E u r o p e a n populations of h o n e y bees (MORITZ, 1986). Estimates f o r h 2 in the n a r r o w sense (selectability) of defensive b e h a v i o u r in the field a n d o t h e r l a b o r a t o r y tests, w h e r e e n v i r o n m e n t a l effects strongly interfere, are substantially smaller or show a large variation (COLLINS, 1982; COOLLINS et al., 1984; RINDERER et al., 1983). The estimate of the genetic variance in the present study, however, m a y be biased since preselected material was tested. This increases the genetic variance in the sample and therefore m a y result in overestimates of the different variance components. Effects of n o n additive gene and genotype interactions were f o u n d to be a m a j o r f a c t o r of the a l a r m reaction in the present study. The estimate

ALARM

304

BEHAVIOUR

IN HONEY

T a b l e I I . - - A N O V A of d i a l l e l s i b - a n a l y s i s , t = f i c a n t , * = p. < 0.01.

BEES

intraclass correlation, ns

=

n o t signi-

Tabelle II. -- Varianzanalyse der diallelen Geschwisteranalyse. t = Intraklasskorrelation, n s = n i c h t s i g n i f i k a n t , * = p < 0.01. Source of variance

df

Mean squares

Variance component

F

t •

SD

Main effects : sires

5

244.51

5.88

22.02 ~

0.18 •

0.07

dams

5

408.68

11.41

36.82*

0.34 •

0.14

I

55.46

----0.23

repl.

queens

< 1 ns

--

Interactions : sire x darn

7

3.99

5.38

4.99*

dam

5

12.55

0.72

1.67ns

--

sire x repl.

5

14.24

0.10

1.28 n s

--

sire x dam

7

1.67

--1.89

< 1 ns

--

x replicate error

144

11.10

11.10

--

--

Total

179

30.21

33.12

Table

x repl.

III. -- Average experiment.

reactions

of

test

groups

[gl02/bee/min]

0.16 •

in

a

cross

0.14

fostering

T a b e l l e I I I . - - M i t t l e r e R e a k t i o n y o n T e s t g r u p p e n (~tl0.o/Biene/min • S E) i m , A d o p t i o n s v e r s u c h . E i w a b e n a u s h o c h (high) u n d s c h w a c h (low) r e a k t i v e n V S l k e r n w u r d e i n unverxvandte h o c h u n d s c h w a c h r e a k t i v e V 51ke r e i n g e h ~ i n g t u n d d i s A r b e i t e r i n n e n 4 Tage nach Schlupf getestet. Genetic mother colony

Foster colony High

Low

A

B

A

B

A

17.8 _+ 2.7

--

18.0 ___ 2.3

--

B

--

High

A

4.9

•

19.1 • 0.9

1.5

--

-4.9

+

19.4

•

2.8

7.0 •

0.6

0.7

Low B

--

6.2 •

1.5

--

R.F.A. MORITZ, E.E. S O U T H W I C K and J.R. H A R B O

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for the i n t e r a c t i o n variance component, however, suffers a high s t a n d a r d error. Classical dominance effects (non-linear gene interactions) m a y be strong in this case, since the interactions between the m e m b e r s of the testg r o u p (genotypes) are mainly linear for this b e h a v i o u r (MORITZ and SOUTHWICK, 1986). Besides the genetic effects we can also see that m a t e r n a l effects m a y play a considerable role in the determination of this c h a r a c t e r (however, due to the large s t a n d a r d error, the estimate is not very accurate). Maternal effects on behavioural and physiological characters of individual honeybee w o r k e r s a n d drones have been r e p o r t e d previously (MoRITZ, 1982, 1985a). Nevertheless it is surprising to find such effects in the social b e h a v i o u r of a group of individuals. Since the effect of c o m m o n hive e n v i r o n m e n t does not significantly affect this b e h a v i o u r in o u r study, the pre-eclosional e n v i r o n m e n t in the colony seems to cause a m i n o r effect only. H o n e y bees are able to maintain an extremely c o n s t a n t intra colonial e n v i r o n m e n t and regulate t e m p e r a t u r e , h u m i d i t y a n d CO2 c o n c e n t r a t i o n accurately (LINDAUER, 1954 ; SOUTHWICK and MUGAAS, 1971; SOUTHWICK, 1985; SEELEY, 1982; RITTER, 1983). This intracolonial h o m o e o s t a s i s m a y reduce the effects of e n v i r o n m e n t a l variation on gene expressions f o u n d in non social insects. Since the estimate of maternal effects is high, previous heritability estimates for o t h e r characters of the honey bee (PIRCHNER et al., 1962 ; SOLLER and BAR COHEN, 1968 ; OLDROYDand MORAN, 1983 ; MORITZ and KLEPSCH, 1985) which do n o t consider this issue, m a y be strongly biased a n d substantially overestimated because of unexpected m a t e r n a l effects. The p r e s e n t results show that these m a y well be within the range f o u n d for m a m m a l s a n d birds. Heritability estimates of defensive behaviour w h i c h rely on the d a m variation only, will not be very accurate when estimating the heritability in the n a r r o w sense. Sib-analysis as suggested by OLDROYD and MORAN (1982) or MORITZ (1986), using the dam variance to estimate the heritability in the b r o a d e r sense (coefficient of genetic determination), should only be used as estimators for hn2, in cases where maternal effects and interactions between genes and genotypes are k n o w n to be small. If there is no previous knowledge, only a nested sibanalysis, which allows the evaluation of the sire variance c o m p o n e n t , will give reliable estimates of the selectability, not biased by m a t e r n a l or pre-eclosional effects. ACKNOWLEDGMENTS.~ We Wish to thank Dr. E.H. ERICKSONand Dr. T.E. RINDERERfor the honey bee material and supplies. Financial support was granted by the Alexander-vonHumboldt-Stiftung (RFAM) and the Research Foundation of the State University of New York.

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