Insec tes Sociaux, Paris 1984, V o l u m e 31, n ~ 4, pp . 375-386

�9 Mas s o n , Par i s , 1984

EVOLUTIONARY GENETICS OF SOCIAL WASPS

(HYMENOPTERA, VESPIDAE, VESPULA) S.L. VARVIO-AHO (1), P. PAMILO (1) (3), and A. PEKKARINEN (2)

(1) Department of Genetics and (2) Department of Zoology, University of Helsinki P. Rautatiekatu 13, SF-O0100 Helsinki 10, Finland

(3) School of Zoology, University of NSW, Australia Regu le 21 sep tembre 1983 Acceptd le 20 juin 1984

S U M M A R Y

Genetic relat ionships of eight nor thern European yellow jacket species, representing Vespula s. str. (the rufa group), Paravespula (the vulgaris group) and Dolichovespula, are here s tudied by enzyme electrophoresis. The observed level of intraspecific genic variation is relatively low, and the southern Finnish populations show no clear-cut geographic differences. The allozyme characters are fur ther used to const ruct phylo- genetic trees by four tree-building techniques. It is suggested that Dolichovespula media is not phylogenetically closely related to other European Dolichovespula species, and that Paravespula and Vespula s. str. may not form a single monophylet ic group. Two of the species studied, V. austriaca and D. omissa, are obligatory social parasites. In both cases the parasi te is related to its host. This supports the hypothesis that the social parasi te generally arises from the same ancestral stock as the host species.

R E S U M E

G6n6tique 6volutive des gu6pes sociales

Les relations gdndtiques de huit esp~ces de gu6pes d 'Europe du nord, reprdsentant Vespula s. str. (le groupe rufa), Paravespula (le groupe vulgaris) et Dolichovespula, sont dtudi6es ici pa r dlectrophor~se enzymatique. Le niveau de variation gdn6tique intrasp6ci- fique observd est relat ivement bas, et les populations du sud de la Finlande ne mont ren t pas de diffdrences gdographiques nettes. Les caract~res d'allozymes sont ensuite utilisds pour construire des arbres phylogdndtiques par quatre techniques de construction. I1 est suggdrd que Dolichovespula media n'est pas 6troitement apparentde aux autres esp6ces de Dolichovespvla europdens, et que Paravespula et Vespula s. str. ne fo rment peut-~tre pas un seul groupe monophyldtique. Deux des esp6ces dtudides, V. austriaca et D. omissa, sont des parasi tes sociaux obligatoires. Dans les deux cas le parasite est apparent6 son h6te. Cela appuie l 'hypoth~se que le parasite social appara~t g6ndralement h par t i r de la m6me souche ancestrale que l'esp~ce h6te.

376 S.L. VARVIO-AHO, P. PAMILO and A. PEKKARINEN

INTRODUCTION

The social wasps belonging to the family Vespidae seem to have originated in East Asia in, or before, the early Tertiary and the diversification to sub- family level has probably taken place in that region (RICHARDS, 1971). The subfamily Vespinae is often divided into three general : Provespa, Vespa and Vespula, all the species being either eusocial or social parasites of their eusocial relatives. The above order also reflects the average distance of the geographic range of distribution of the present day species from their hypo- thesized region of origin.

The Vespula wasps comprise a group of over 30 Holarctic species and are fur ther divided into Vespula (rufa group), Paravespula (vulgaris group), and Dolichovespula, which differ from each other on the basis of both mor- phology, nesting habits and behaviour (e.g. SPRADBERY, 1973; GREENE, 1979). In the present paper, we use these names without specifying whether they should have generic or subgeneric status (cf. SPRADBERY, 1973 ; JEANNE, 1980). We use the term Vespula coll. to denote the whole groupe and to distinguish if from Vespula in the sense of the rufa group.

BLi.iTHGEN (1961) suggested that the social parasites should be placed in different general from their host species, but t~is view has been generally rejected and, indeed, it has been recognized from the very first studies of social parasitism that the parasite and its host are often closely related to each other (RoBsoN, 1898; CARPENTER and PACK-BERESFORD, 1903; TAYLOR, 1939). The phylogeny suggested for the European species by de BEAUMONT (1958) on the basis of copulatory organs also indicated close relationships between the social parasites and their hosts (fig. 1A)

If the characters used to reconstruct phylogeny are subject to selection pressures, the conclusions will be biased because of either convergent or divergent evolution. And even though some morphological characters, like male copulatory organs, are often considered as suitable for determining phylogenetic relationships, they do not lend themselves easily for estimating the degrees of difference in terms of evolutionary time. On the other hand, it is widely accepted that biochemical evolution at the level of genes and their pr imary products, proteins, can be used as a rough molecular clock reflecting evolutionary history (e.g. NEI, 1975; WILSON et al., 1977). In this paper we take this approach and use electrophoretically studied enzyme gone differences to construct a phylogeny of northern European yellow- jackets (Vespula co11.). The special problems we examine here are the level of intraspecific genetic variation, the genetic affinities of the suggested genera or subgenera, and the origin of social parasitism in these wasps. A brief account of the results has been earlier reported by PAMILO et aI. (1981).

E V O L U T I O N A R Y G E N E T I C S O F S O C I A L W A S P S 377

M A T E R I A L S A N D M E T H O D S

The mate r i a l was collected in sou thern Fin land f rom Espoo, Hanko, Helsinki and Tuusula, and i t consis ts solely of diploid individuals ( t a b l e I ) . The mater ia l was so collected t h a t the individuals are likely to come f rom different nests. The Hanko mater ia l was par t ly collected in late spr ing/ear ly s u m m e r and consis ts of migra t ing queens (see MIKKOLA, 1978 for the migrat ions) .

E lec t rophore t ic samples were p repared by grinding the head and thorax of each individual in 0.3-0.5 ml distil led wa te r and the homogena te was used for electrophoresis . The buffers used in hor izonta l s ta rch gel e lectrophoresis were (A) e lec t rode : 135 mM Tris-HC1, pH 7.1, gel : di luted in 1 : 15 f rom the electrode buf fe r (AYALA e t a l . , 1972), and (B) e lec t rode : as in A, gel : 43 mM Tris-HC1, pH 8.4 (VARvIo-AHo and PAMILO, 1980). The e lect rophoret ic runs of 14 % (w/v) s ta rch gels were done using a cons tan t voltage 6 V/cm, approximate ly for 6 hours.

Table I. - - Mater ia l used for the present study, all individuals are diploid.

Tableau I. - - Mat6riel utilis6 pour la pr6sente 6tude, t o u s l e s individus 6tant diploides.

Species Helsinki Hanko Espoo Tuusula

V . r u f a 7 41 11 - -

V . a t t s t r i a c a 2 8 - - - -

P . w d g a r i s 10 17 54 18

D. s a x o n i c a 14 35 3 - -

D. s y l v e s t r i s - - 9 - - - -

D . n o r w e g i c a - - 4 - - - -

D . o m i s s a 1 - - - - - -

D. m e d i a ~ - - - - 2

The enzymes stained, using mainly the methods of AYALA e t al . (1972), were f rom buffer System A : alpha-geycerophosphate dehydrogenase (GPD), es terase (EST) and mala te dehydrogenase (MDH), and f rom buffer B : aldehyde oxidase (AO), hexokinase (HK), isoci t ra te dehydrogenase (IDH), leucine aminopept idase (LAP), malic enzyme (ME), phosphoglucomutase (PGM), phosphoglucoseisomerase (PGI), and glyceraldehyde-3-phos- pha t e dehydrogenase (G3PD). Amylase (AMY) was scored as t rans lucen t bands from LAP gels. Not all the enzymes could be scored f rom all the individuals, not even f rom all the species, because of fa int or too diffused staining, or lack of mater ia l . EST, GPD, HK, LAP and MDH showed two zones of isozymes which were scored as produc ts of two separa te loci. The loci are denoted by hyphena ted numbers , n u m b e r 1 being the mos t ca thodal one. The anodal MDH-2 showed mult iple bands in some species, and the scoring has been done on the basis of the m a j o r band.

R E S U L T S

1. I n t r a s p e c i f i c v a r i a t i o n

T h e m a t e r i a l w a s n o t s p e c i a l l y c o l l e c t e d f o r e s t i m a t i n g l e v e l s o f g e n i e

v a r i a t i o n b u t a l l o w s s o m e e s t i m a t e s f r o m t h e l a r g e s t s a m p l e s ( t a b l e I I ) .

378 S.L. VARVIO-AHO, P. PAMILO and A. P E K K A R I N E N

We have previously reported genetic monomorph i sm in southern Finnish P. vulgaris (PAMILO et al., 1978). That material is par t of our present results, but in addi t ion to that we have found slight heterozygosity at three loci in the Espoo populat ion, namely at IDH, MDH-1, and HK-2. The frequency of the commones t allele is .96, .92 and .99, respectively. Vespula rufa had four polymorphic enzymes. The frequency of the commones t allele was in the Hanko sample 0,93 at PGI and 0.81 at EST-1, and in the Espoo sample 0.68 at PGI, 0.89 at LAP-I, and 0.57 at ME. In D. saxonica we had samples both f rom Hanko and Helsinki. The Hanko sample had polymorphic HKol, with allele frequencies 0.63 and 0.37. The Helsinki sample had polymorphic PGI with the f requency 0.9 of the commones t allele. Of D. sylvestris we had only nine individuals f rom Hanko, and they had polymorphic ME and GPD-1 with the f requency of the commonest allele being 0.75 and 0.83, respectively. D. norwegica had one heterozygote at ME, but in the very small samples of D. media, D. omissa and V. austriaca we found no variation.

Table II. - - Observed enzyme genic variation in the population samples ; H is the expected mean heterozygosity per locus.

Tableau II. -- Variation gdnique enzymatique dans les 6~:hantillons de population: H est la moyenne d'hdtdrozygotie attendue par locus.

Species Population No. of loci

Total Polymorphic H

V. rufa Hanko 14 2 .031 Espoo 10 3 .113

P. vulgaris Helsinki 11 0 0 Hanko 12 0 0 Espoo 12 3 .020 Tuusula 11 0 0

D. saxonica Helsinki 12 1 .015 Hanko 14 1 .033

D. sylvestris Hanko 13 2 .050

No clear geographic differences were detected w i t h i n the species : the commones t allele was always the same in the different areas. The lack of geographic differentiation in the scale studied here is quite expected when we recall that the wasps have large-scale migrat ions (RuD~ECK, 1965; MIrrOLA, 1978) and such migrations are likely to wipe out any local gene f requency differences. As our material in MIKKOLA (1978) shows, the spring migrat ions include queens with undeveloped ovaries f rom V. rufa, D. saxonica, and apparent ly also P. vulgaris, D. sylvestris and D. norwegica. We have also observed summer migrations of D. sylvestris in TvSrminne archipelago in Hanko in early July 1977. The wasps were accompanied by LibeUula

EVOLUTIONARY GENETICS OF SOCIAL WASPS 379

dragonfl ies ; m i d s u m m e r migra t ions of Libellula have been repor ted earl ier b u t those r epor t s do not ment ion social wasps (NORDMAN, 1935).

2. Interspecific differences

As the level of enzyme gene var ia t ion is ra ther low in the species studied, the s tudy of in terspecif ic re la t ionships can be based on ra the r small samples.

The al lozymic compar i sons are done by denot ing the m o s t c o m m o n e l e c t r o m o r p h of P. vulgaris by 100. The e l ec t romorphs of the o ther species a r e denoted by n u m b e r s depending on the e lect rophoret ic mobi l i ty of the values re fe r to the mi l l imetr ic difference in mobil i ty unde r our s t andard running condi t ions (table III). On the basis of the prevalent e lec t romorphs , all the species can be told apa r t f rom each other. In fact, D. omissa shares no e l ec t romorphs in c o m m o n wi th the two Vespula species rufa and austriaccu

Assuming tha t each e l ec t romorph represents a specif ic allele, we can e s t ima te genetic dis tances be tween the species pairs f rom the allele frequen- cies (we use only the loci given in table III). There are several me thods for es t imat ing this distance, we use here NEI ' s (1975) s tandard genetic distance, D = - - logI, where I is the genetic identi ty be tween species. This es t imate ref lects evolu t ionary t ime, assuming that genetic di f ferent ia t ion is mainly due to genetic dr i f t and increases at a constant rate. When calculat ing the d is tance es t imates , we pooled our mater ia l together f rom all the localities. When the overal l ident i ty is zero, the distance becomes inf in i te ; be low we rep lace such es t imates by the greates t distance found be tween the o ther species pa i r s when the distance mat r ix is used for es t imat ing the phylogeny. The mat r ix of genetic dis tances (table IV) shows some appa ren t c luster ings of species but there are two species, P. vulgaris and D. media, which are not closely re la ted to any of the o ther spec ies in this study.

3, Phylogenetic construction

There are var ious techniques for generat ing a plausible phylogeny f rom the genetic data. We have used the following four t echn iques : 1. UPGMA clus ter ing (SNF_ATH and SOKAL, 1973); 2. LYS (1981) me thod which modif ies the UPGMA techn ique ; 3. Fitch-Margoliash t echn ique ; and 4. Wagner par- s imony technique. Techniques 1-3 use the genetic distance ma t r ix (table IV), a n d the Wagner technique uses the allelic data coded in 0,1 f o r m a t (i.e. 0 = allele is absent , 1 = allele is p resen t in the given species, used here only fo r the p reva len t alleles given in table III). For the me thods 3 and 4 we used the c o m p u t e r p rog ram s of the p r o g r a m package PHYLIP 2.2 made avai lable by Dr. FELSENSTEIN, the techniques have recent ly been reviewed b y FELSENSTEIN (1982).

380 S.L. VARVIO-AHO, P. PAM[LO and A. P E K K A R I N E N

~

E V O L U T I O N A R Y G E N E T I C S OF S O C I A L W A S P S 381

Table IV. - - Nei's standard genetic distances (the upper half) between the species pairs, calculated from pooled data, and the number of loci (the lower half) used in these comparisons.

Tableau IV. m Distances g6n6tiques standard de Nei (la moiti6 sup6rieure) entre les esp~ces appareilldes, calcul6es h partir de donn6es group6es ; et nombre de loci (la moiti6 inf6rieure) utilis6 pour ces comparaisons.

rufa aust vulg saxo sylv norw omis medi

V. rula 0.11 1.47 2.54 1.11 2.07 oo 1.43 V. austriaca 10 1.20 2.30 0.71 0.92 ~ 1.25 P. vulgaris 13 10 1.18 1.29 1.32 1.39 2.20 D. saxonica 13 10 13 0.34 0.26 0.13 2.20 D. sylvestris 12 10 12 12 0.52 0.43 1.90 D. norwegica 8 5 8 8 7 0.29 1.79 D. omissa 8 7 8 8 8 4 1.95 D. media 9 7 9 9 8 6 7

Of the me thods used, UPGMA and LI 's m e t h o d p roduce a roo ted tree, whereas the o t h e r two give a ne twork wi th b ranch ing bu t do not a l low d rawing a d i r ec t ed tree. UPGMA is a pheno typ ic c lus te r ing technique and p roduces a phene t i c dendrogram, a phenogram. This p h e n o g r a m can be i n t e r p r e t e d as an evolu t ionary t ree when we assume tha t each l ineage evolves at the same ra te (see e.g. BERLOCHER and BUSH, 1982). LI ' s m e t h o d is o therwise very s imi la r to UPGMA, bu t i t a l lows d i f ferent evo lu t ionary ra t e s among the l ineages. The shape of the t rees genera ted f rom our ma te r i a l by these two ou r m a t e r i a l by these two techniques are ident ical , the only d i f ferences being in the b ranch lengths fig. 1C, D). Of the ne t work-c rea t ing p rocedures , the Fi tch-Margol iash gave a banch ing o r d e r ident ica l to tha t of the two t rees (fig. 1E), whereas the species group norweg ica - saxon ica - o m i s s a is r e o r d e r e d in the Wagner ne t w or k (fig. 1F). The b r a n c h lengths for the W a g n e r n e t w o r k are here e s t ima ted by solving the m i n i m u m n u m b e r of al lel ic changes wi th in the network. When doing this, we a s sume tha t each allele ( recognized on the basis of the co r re spond ing e l ec t romorph) can m u t a t e to any of the o ther p resen t in the group. When it was not poss ib le to resolve exact ly where the muta t ion had taken place, we a d d e d 0.5 uni ts in bo th i n t e rnoda l d is tances concerned (or 1/3 if the re a re th ree poss ibi l i t ies) .

The p r o p o s e d evolu t ionary t ree shows some c lus ter ings of species. The two species of V e s p u l a s. str . c lus ter t ight ly toge the r and the species of D o l i c h o v e s p u l a c lus te r together , except D. media . In fact, the l a t t e r spe- cies was the m o s t d i f ferent f rom all the o the r wasps in this s tudy, showing g rea t genet ic d i s tances f rom them. When looking f rom the roo t of the tree, D. m e d i a and the o ther Dol ichovespu la species are in d i f fe ren t ma in bran- ches, and the same holds for Ve spu la s. s tr . and Paravespu la .

382 S.L. VARVIO-AHO, P. PAMILO and A. P E K K A R I N E N

/ crabro l ~ ~ ~ ~ ~ ~ ~ j ~ ~ ~ / m e d i a o ,~,- oC~

~ / sylvestris ~ ~ o ~ ~ c~ ~ ^ r / / / . . . omissa ~ ( ~ I ~'~ l X I

~ c hov.~j..~ adulter,n a > - ~ '- ~" ~ E ~ ~ a • ~ ~ norweglca

~ vutgaris /"o ~-"~_ ~ germanica ~'SD O ~ rufa

"O ~ aus~Daca

A. de Beaumont 1958 ~. Yamane 1976

media --[ rufa austrJaca sylvestris ~ _j~ saxonica

I omisso norwegico vulgaris

C. UPGMA

7 edia

/ ~'~...austriac a ~rufa

~ vulgaris

~'----...s yl ve st r is . ~no rweg l ca

~-~..~omissa ~. Li soxonica

i/)

~n

D O O > O O u O o u ~

�9 ~_ ,~ "~' ~ o "

o ~ OX~

0 C O ' - - 0

E. Fitch - Nargoliash

D >

oo "7- ~

[2. Wagner

Fig. i. - - Yellowjacket phylogenies suggested on the basis of morphological and behavioura l charac te rs by A) DE BEAUMowr (1958), and B) YAMANE (1976), and on the basis of p resen t e lectrophoret ic resul ts using C) UPGMA, D) LI, E) FITCH- MaRCOLr~SbI, and F) WACNER tree-building techniques. The trees E and F are unrooted.

Fig. 1. - - Phylogen6ses des gu6pes sugg6r6es h pa r t i r de caract6res morphologiques et et compor t emen taux pa r A) DE BEALrMowr (1958) et B) YAMAME (1976) et h pa r t i r des pr6sents r6sul ta ts 61ectrophor6tiques en ut i l i sant les techniques de cons t ruct ion d ' a rb res de C) U ~ , D) LI, E) FITC~t-MARC, OLIASn et F) WACNER. Les a rbres E et F ne sont pas enracin6s.

EVOLUTIONARY GENETICS OF SOCIAL WASPS 383

Two of the species s tud ied here are social pa r a s i t e s : V. austriaca of V. ru/a and D. omissa of D. sytvestris (de BEAUMONT, 1958). In bo th cases the paras i t e and its host are closely re la ted to each other, a l though D. omissa is not the closest ally of D. sylvestris. De BEAUMONT also noted, on the basis of morphologica l charac ters , tha t D. omissa is closer to D. saxonica than to D. saxonica than to its own hos t species.

D I S C U S S I O N

The var ious phylogeny-generat ing techniques gave congruen t resul ts and the rel iance on the p resen t resul ts hence depends on our data. The r a t he r low heterozygosi ty and lack of clear-cut geographic di f ferences pa r t ly jus t i fy our use of small samples (which means tha t the resu l t s largely depend on the preva len t alleles), bu t we have to note tha t the mate r ia l comes f r o m geographical ly res t r ic ted area. A far m o r e crit ical f ac to r is the small n u m b e r of loci used, and the interspecif ic compar i sons come pa r t ly on different sets of loci. This suggests tha t we cannot be conf ident of the mino r details of the p roposed evolut ionary trees, a l though there are some evident pa t t e rns which we can discuss reliably.

I t is general ly considered that the vespine genera Provespa and Vespa have m a n y pr imi t ive features, bo th morphologica l and behavioural , indi- cat ing that the genus Vespula coll. has derived f rom Vespa-like ances tors (fig. 1A, B; RICHARDS, 1971). Although Vespula coil. is cons idered as a monophyle t ic group, GREENE (1979) notes that the evidence is not decisive because " there are fewer derived vespine charac te r s ta tes shared by all ye l lowjackets than might be expected ". Within yel lowjackets , Dolichoves- pula shares m a n y fea tures wi th Vespa, and this has led GREENE (1979) to suggest tha t Dolichovespula is a pr imi t ive group in yel lowjackets , and tha t Vespula and Paravespula fo rm a monophyle t ic group which evolved f r o m the Dolichovespula stock.

The obse rved genetic heterogenei ty within Dolichovespula, caused by D. media, indicates tha t this group may not be monophyle t ic bu t consists of those yel lowjackets which have re ta ined some pr imi t ive charac te r s (on the o ther hand, YAMANE (1976) concludes tha t Do lichovespuIa species share some derived larval charac te r s tates and are less re la ted to Vespa than the o the r ye l lowjackets are, fig. 1B). Unfortunately, our s tudy includes only one Paravespula and two VespuIa s. str. species, and it is imposs ib le to say how tight c lusters these taxa form. JACOBSON et al. (1978) have examined Nor th Amer ican Paravespula species e lect rophoret ical ly and on the basis of 13 enzymes they concluded tha t the five species examined (vuIgaris, germa- nica, pensyIvanica, maculifrons, and flavopitosa) f o r m a t ight c lus ter of re la ted species. I t seems mos t likely tha t the Vespula and Paravespula

384 S.L. VARVIO-AHO, P. PAMILO and A. PEKKARINEN

groups can be regarded as dis t inct groups, a l though the classification of the species V. squamosa and V. sulphurea is yet unclear (MacDONALD et al., 1976). I t is l ikely that bo th Paravespula and Vespula s. str. are monophy- lefic, and the present results indicate that these two groups have originated separate ly f rom Dolichovespula-like ancestors. The root of the UPGMA tree is a t the distance D = 1.92. I f we use this genetic distance as a mole- cular clock wi th one unit represent ing approximate ly 14 million (MAxsON and MAXSON, 1979) to 18.9 million years (VAWTER et al., 1980), this dates the origin of yel lowjacket diversification i n mid Tert iary. However, a small n u m b e r of loci does not allow f i rm conclusions, and the scale of the clock is still disputed.

GREENE (1979) suggests that Vespula (in the sense of tu fa group) may have or iginated in Nor th America ; if Paravespula is an Old World g ro u p , this could suppor t our conclusion. Although Dolichovespula differ f rom o ther yel lowjackets in many respects (GREENE et al., 1976; GREENE, 1979), ou r resul ts point to internal heterogenei ty within this group. To resolve the phylogeny of these groups, we should include both nearct ic and palearct ic species in the s tudy and use Vespa hornets for outgroup comparisons. I t is also in teres t ing to note that YAMANE (1976) regards V. rufa and D. sylves- tris as in te rmedia te forms between Paravespula and Dolichovespula. Our present resul ts indicate that V. rufa is genetically more closely related to D. sylvestris than to any o ther Dotichovespula, and the two species showed mult iple banding pat terns in the anodal MDH-2 (see above).

One impor t an t conclusion f rom our genetic studies is that the two social parasi tes examined originate f rom the same evolut ionary lineages as thei r hosts. This renders baseless those taxonomic subdivisions which separa te the parasi t ic species into (sub) genera different f rom their hosts (e.g. WEYRAUCH, 1937 ; BLi.iTHGEN, 1961).

We can conclude that the proposed phylogeny of vespine wasps offers a good evidence for the evolution of social parasi t ism according to the so called Emery ' s rule. EMERY (1909) s tated that the most plausible route for social paras i t i sm to evolve is that the parasi te and its host have their origin in the same ancestral stock. EMERY presented this hypothesis mainly for ants, bu t TAYLOR (1939) has fu r the r discussed the possible routes of this evolut ion in social wasps and suggests a series of four stages in the evolu- t ionary pa thway of paras i t i sm: intraspecif ic and interspecific facultative t empora ry parasi t ism, obligatory t empora ry paras i t ism and obligatory per- manen t parasi t ism. This series of evolut ionary steps makes it understan- dable tha t the social parasi te and its host are expected to be close relatives, a l though in the case of V. squamosa (which is a social parasi te of Paraves- pula maculi[rons) this is not the case (MacDONALD and MATTHEWS, 1975; MATTHEWS, EPFLJ. The behavioural studies of social parasi t ism indicate that the parasi t ic D. arctica queen uses at least par t ly chemical control over the

E V O L U T I O N A R Y GENETICS OF SOCIAL W A S P S 385

host worke r s (GREENE et al., 1978), bu t there seem to be differences be tween the species, V. austriaca and V. squamosa queens showing m o r e aggressive physical dominance than D. arctica (REED and AKRE, 1982 ; MATTHEWS, 1982). On the basis of TAYLOR'S hypothesis , we could expect the use of chemical controI , o r the o the r way round we could say that p h e r o m o n a l s imilar i ty of closely re la ted species offers a mechan i sm leading to TAYLOR'S hypothesis . This still leaves it open whe ther obl igatory social paras i t i sm, inquil inism, has ar ised by sympa t r i c speciat ion (STARR, 1979).

Even though social pa ras i t i sm would arise in closely re la ted species, it need not p red ic t that the existing parasi te-host pairs should always fo rm a dist inct two-species clusters the phylogenetic tree. We know tha t social pa ra s i t i sm is a f requent phenomenon in social insects (see RICHARDS, 1971 ; WILSON, 1971; MICHENER, 1974), and we would expect tha t in some cases pa ra s i t i sm is quite ancient. There may be some cases in vespine wasps falling in this category, but not as clearly as in bumblebees (PAMILO et al., 1981). This suggests that the extinction rate is high among the social para- sites (this can be predic ted f rom fluctuat ions of the popula t ion size, p robab ly associa ted to social pa ras i t i sm (MATTHEWS, 1982)), and the cases we see today rep resen t r a t he r recent evolution.

ACKNOWLEDGMENTS. - - We thank Dr. R.H. CROZIER for comments on the manuscr ipt . The study has been financially supported by the Finnish Cultural Foundation, the Emil Aaltonen Foundation, and the National Research Council of Sciences of Finland.

References

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