Table Of ContentHYM. RES.
J.
Vol. 4, 1995, pp. 41-63
The Last Twenty Years of Parasitic Hymenoptera Karyology:
An Update and Phylogenetic Implications
Vladimir E. Gokhman and Donald L. Quicke
J.
(VEG) Botanical Garden, Moscow State University, Moscow 119899, Russia;
(DLJQ) Department of Biology, Imperial College at Silwood Park, Ascot, Berks SL5 7PY, U.K.
—
Abstract. A survey of karyological data in the parasitic Hymenoptera shows a considerable
uniformity in chromosome numbers within higher taxonomic groupings, with most chalcidoids
having n = 5-6 and most cynipoids, ichneumonoids and those very few species of Diapriidae
and Scelionidaeexamined to date havingn = 10-12. The Encyrtidae and Eurytomidaediffer from
other chalcidoids examined to date in having higher n values (8-11). The braconid subfamilies
Aphidiinae {ii - 4-7), Charmontiinae (n = 5) and Exothecinae (» = 6) are shown to have lower
values than do otherbraconids. New data are presented for 32 species, including the first records
ofchromosomenumbersfortheEupelmidae,Bethylidae,Diapriidae,Ormyridae,the ichneumonid
subfamilies Banchinae, Pimplinae, and Tryphoninae, and the braconid subfamilies Aphidiinae,
Charmontinae, Doryctinae, Exothecinae, Macrocentrinae, Meteorinae, and Miracinae. Chromo-
some number data are discussed in relation to current views on Hymenoptera phylogeny.
INTRODUCTION menopteran chromosomes (Imai et al.
1988, Baldanza et al. 1991b), have opened
There has long been a tendency for tax- the possibility of greatly expanding our
oofnosmyissttesmattoicigenvoiredemnacenyinpoftaevnotuiralosfoumrocrees Fkunrotwhlere,dgiteisofnopwarapsoistsiicblweatsopobktaariynolgoogoyd.
traditional morphological, and nowadays results working with adult tissues such as
molecular, data. Whilst this lack has not ovaries (Gokhman 1985, 1990a), and such
been ubiquitous amongst taxonomists, protocols have allowed, for the first time,
where it has occurred it may have been an examination of chromosome number
due to a number of reasons including lack and structure in natural populations.
of understanding of novel characters, lack Karyological studies have, nevertheless,
of facilities for investigating them and lack played an important role in the systemat-
of availability of information about such ics and species level taxonomy of various
characters. In this respect, it is not sur- groups of the non-parasitic Hymenoptera
prising that chromosome number and oth- including, sawflies, ants, bees and social
er karyological features have played little wasps (principally Polistinae) and these
role in considerations of hymenopteran have been reviewed in detail elsewhere
phylogeny, and this is especially true for (see for example, Kerr 1972, Kerr and da
the parasitic families. Reasons for this are Silveira 1972, Naito 1982, Imai et al. 1977,
manifold. Hymenopteran chromosomes Moritz 1986, Pompolo and Takahashi
have traditionally been studied in imma- 1987, 1990, Hoshiba, Matsuura and Imai
ture stages in which dividing cells are 1989, Costa et al. 1993). Wide variation in
common, but larvae ofparasitic wasps are n is well known among the ants (Formic-
perhaps especially difficult to identify and idae) and ranges from 1 to 47 (Imai and
obtain except when species are in culture. Taylor 1989, Imai et al. 1990), but is modal
Recent developments in the study of hy- at 11 (Imai et al. 1988). Indeed, the greater
42 Journal of Hymenoptera Research
part of this range can even be found with- tory cultures. Chromosome preparations
in the single ant genus Myrmecia. How- were obtained according to the schedule
ever, within the parasitic Hymenoptera described in Appendix I. Voucher speci-
there appears to be be rather more consis- mens for Ichneumoninae are deposited in
tency, and for most famiUes the observed the collection of Moscow State University,
range of variation is far narrower. those for other taxa are in the Natural His-
Outside of the Hymenoptera,both chro- tory Museum, London.
mosome numbers, structure and size have RESULTS AND DISCUSSION
all been found useful in phylogenetic re-
construction, usually but not exclusively The last review of chromosome number
in combination with other morphochar- in the parasitic Hymenoptera was by Cro-
acters, and this has been particularly true zier (1975) at which time values were
of plant systematics. For example, George known for only about twenty species
& Geethamma (1992) have recently pro- (with data published before 1930 not in-
posed a phylogeny of jasmines based on cluded for the reason of insufficient reli-
chromosome numbers and assumed poly- ability); his data are summarized in Figure
ploidy events. Among the insects, chro- 1. Since then, chromosomes of nearly 140
mosome numbers have been used exten- additional species have been studied
sively in the systematic treatment and (Gokhman 1994), and for this review we
phylogeny of the Hemiptera (Blackman have investigated 32 more in order to help
1980, Emeljanov & Kirillova 1989, 1991). fill in a number of gaps and to confirm
Kuznetsova (1985), for example, has con- some previous findings. These data are
cluded that the homopteran subfamily Or- presented in Table 1 and summarized in
geriinae is monophyletic based on an au- Figure 2. The great majority of published
tosomal fusion giving 2m=27 (in males) chromosome numbers come from studies
compared with the plesiomorphic value of on the ichneumonid subfamily Ichneu-
2n=29 (in males), and similarly that the moninae by Gokhman (1985, 1987, 1989,
tribe Almanini of the Orgeriinae is mono- 1990a, 1990b, 1991a, 1991b, 1993a), though
phyletic on the basis of an autosome-sex they also include a substantial body of ev-
chromosome fusion (giving 2n=26). idence especially relating to various fam-
In this paperwe review the currentstate ilies of Chalcidoidea. Within the better
of knowledge of the karyology ofparasitic studied parasitoid families (i.e. Ichneu-
wasps and, in addition, provide new data monidae, Cynipidae, Torymidae) chro-
for approximately 32 taxa including the mosome numbers were found to be rela-
first records of chromosome numbers for tively stable, and were generally uniform
the Eupelmidae, Bethylidae, Diapriidae, at the generic level. This contrasts mark-
Ormyridae, the ichneumonid subfamilies edly with observations for many aculeate
Banchinae, Pimplinae, and Tryphoninae, Hymenoptera which often show striking
and the braconid subfamilies Aphidiinae, chromosomal variability even within gen-
Charmontinae, Doryctinae, Exothecinae, era (Imai and Taylor 1989, Imai et al.
Macrocentrinae, Meteorinae, and Miraci- 1990).
nae. The apparent bimodality in haploid
MATERIALS AND METHODS number of parasitic Hymenoptera appar-
ent in Crozier's small sample (Fig. 1) now
New karyotypic data were obtained us- appears to be well founded (Fig. 2). How-
ing ovarian tissues of adult wasps which ever, the exact modal numbers are slightly
were either collected from the wild at Sil- different (n = 5 and 11 compared with n
wood Park, Berkshire, U.K., during early = 5 and 10 of Crozier), probably due to
September 1995, or obtained from labora- the strong bias in favour of the ichneumo-
Volume 4, 1995 43
14 -T-
12 -
10
6 -
2 --
+ + + +
4-
3 4 5 6 7 8 9 10 11 12 13 14 15 16 17
Haploid chromosome number
Fig. 1. Histogram of haploid chromosome numbers for parasitic Hymenoptera, data modified after Crozier
(1975) to take into account subsequent taxonomic changes.
nid subfamily Ichneumoninae in the pres- monoids whose haploid n values range
ent enlarged data set. As will be apparent from 8 to 17.
ufersomartoheunfdigu5relsa,rgtehleypceoamkpriinsehsapmloeimdbevarls- GENOMIC SIZE AND ITS
of the Chalcidoidea and there is only IMPLICATIONS
slight overlap between these and the other Rasch et nl. (1975, 1977) calculated the
peak centred around 11. The same is true, haploid genomic size of the braconid
though less pronounced, when the data wasps, Habrobracon juglandis and H. seri-
are plotted for genera rather than species nopae both to be 0.154).16 x 10 ^^g dNA
(Figure 3: each n value in a genus being and that of the pteromalid, Nnsonin (as
represented only once in the histogram). Mormoniclla) vitripennis to be 0.33-0.34 X
Members of three of the chalcidoid fami- 10 '-^g. These values translate (using an
lies investigated to date, the Eurytomidae average molecular weight of a base pair
(Eiiri/toma), Encyrtidae (6 species in three as 660) to base pair numbers of approxi-
genera) and Aphelinidae (one species, mately 1.4 X 10** and 3.0 X 10^ base pairs
Pteroptrix (= Archenomiis) orientalis Silves- for the ichneumonoid and the chalcidoid
tri, out of 5 investigated; see below) differ respectively. More recently. Bigot et al.
from other chalcidoids in having haploid (1991) using DNA reassociation kinetics
numbers rangingbetween 8 and 11, whilst calculated the haploid genomic sizes of
members of the braconid subfamilies the ichneumonid Diadroniiis and
piilchclliis
Aphidiinae {Aphidius, Diaretiella, Ephcdriis, the chalcidoid, Eiipclmus viiillcti, as 1-2 X
Praon), Charmontinae [Charmon) and Ex- 10'^ base pairs and 10 X 10"^ base pairs re-
othecinae [Rhysipolis) are atypical in hav- spectively. Unfortunately, no data for the
ing haploid numbers of 4 to 7, 6 and 5 numbers ofchromosomes are available for
respectively, compared with other ichneu- Eupelmus vuiUeti but we have investigated
44 Journal of Hymenoptera Research
Table 1. Chromosomenumber in parasiticwasps
Taxon 2/!* Reterence(h)t
Diaprioidea
Diapriidae
Beli/ta depressa Thomson 8 16 present papertt
Cinetus lanceolatus Thomson 10 20 present paper
Scelionoidea
Scelionidae
Telejtomusfariai Lima 10 20 Dreyfus & Breuer 1944
Chalcidoidea
Aphelinidae
Apheliniis mali Haldeman 5
Aphytis mytilaspidus (Le Baron)
Archenonnis orientalis Silvestri
Encarsia berlesei Howard
Encarsia pergandiella Howard
Chalcididae
Bradiyineria intermedia Nees
B. lasus Burks
B. ovata Say
Dirhiniis himalayanus Westwood
Encyrtidae
Dalman
AgeniaspisfiiscicoUis
Copidosoma buyssoni Mayr
C. gelechiae Howard
C. gelechiae Howard
C. truncatelliim (Dalman)
(= Ifloridanum Ashmead)
C.floridanum Ashmead
C.floridanum Ashmead
Apoanagyrus lopezi (DeSantis)
Eulophidae
Cirrospilus diallus Walker 6
Colpoclypeiisflorus Walker 6
Melittobia chalybii Ashmead 5
Tetrastichusgigas Burks 6
T. megachilidis Burks 6
Eupelmidae
Anastatus catalonicus Bolivar 5
Macroneura vesicularis (Retzius) 5
Eurytomidae
Eudecatoma bigidtata (Swederus) 9
Eurytoma californica Ashmead 10
Leucospidae
Leucospis affinis Say
Ormyridae
Ormynis sp. ?6
Pteromalidae
Anisoptcromalus calandrae (Howard) 7
Coelopisthia extenta (Walker) 5
Dibrachys sp. 5
Lariophagus distinguendus Foerster 5
Muscidifurax zaraptor Legner 5
Nasonia vitripennis (Walker) 5
Volume 4, 1995 45
Table 1. Continued
Taxon Reference(s)t
Nasonia vitripennis (Walker)
46 Journalof Hymenoptera Research
Table 1. Continued
Taxon
Volume 4, 1995 47
Table 1. Continued
Taxon Ret'erence(s)+
Ephialtes manifestator (L.)
48 Journal of Hymenoptera Research
Table 1. Continued
Taxon
Volume 4, 1995 49
30 T
25 -
20 -
15 -
10
7 8 9 10 11 12 13 14 15 16 17
chromosome number
Haploid
Fig. 3. Histogram of haploid ciiromosome numbers of parasitic Hymenoptera, data from Table 1, each n
value occurring in a genusbeing represented only once.
two other eupelmid species in the genera would be interpreted as the application of
Macroneura and Anastatiis, which were the much decried commonality principle.
both found to have haploid numbers of 5 The 'common equals primitive' associa-
in common with Nasonia. Although the re- tion is of course probabilistic rather than
sults of Raschet al. (1975, 1977) and of Big- deterministic (Watrous and Wheeler 1981,
ot et al. (1991) don't quite agree in the or- Frohlich 1987, Quicke 1993). Some further
der of magnitude of base pairs they esti- insight into whether modal chromosome
mate, probably due to differences in pro- number is likely to reflect the ancestral
cedure, they did both show the chalcidoid number can come from the comparison of
to have a larger genome than the ichneu- modal and median numbers. If these
monid. Thus, if these values are roughly numbers coincide, and the whole distri-
representative of other members of their bution may be approximated to a normal
superfamilies, then the chromosomes of one, then the data provide no evidence of
most chalcidoids would be expected to a directed change, though it must be re-
have between four and twenty times as membered that there is always the possi-
much DNA on average thanchromosomes bility that an evolutionary change in chro-
of ichneumonids. mosome number early in the evolution of
CHROMOSOME NUMBER IN the group could lead to the same distri-
bution. In the Ichneumonoidea and the
RELATION TO
HYMENOPTERA PHYLOGENY Cynipoidea both the median and modal
chromosomenumbersare the same 11 and
In karyological studies it is common 10 respectively; in contrast, for example,
practice to interpret modal chromosome ants (Formicidae) have a modal numberof
numbers as representing the initial (ances- 11 but the median is 15. However, cladis-
tral) number, though to many cladists this tic analyses based on independent char-
50 Journalof Hymenoptera Research
acter systems, via outgroup comparisons, the bulk of the taxa currently regarded as
provide the most reliable means of deter- 'Microhymenoptera' including Chalcidoi-
mining plesiomorphic chromosome num- dea, Cynipoidea, Scelionoidea, Diaprioi-
bers and, where possible, this is the ra- dea and Proctotrupoidea s.s. (Fig. 4).
tional that we have employed. Our data show that the modal n value
According to currently accepted views in the Ichneumonoidea, theprobable sister
of Hymenoptera phylogeny, the sawflies group of the Aculeata, is 11. Further, our
('Symphyta') form a paraphyletic group limited data for the less derived aculeates
with respect to the Apocrita with the latter of the family Bethylidae {Epyris and Lae-
being the sister group of the Orussidae, liiis; Fig. 10), whilst demonstrating some
and the Apocrita+Orussidae in turn most degree of variation in haploid number be-
probably being the sister group of the tween 10 and 14, when considered togeth-
Xiphydriidae (Konigsmann 1977, Rasnit- er with data for other aculeates suggest
syn 1980, 1988, Gibson 1985). Unfortunate- the ancestral aculeate may have had a
ly, chromosome numbers are not known haploid number around 11, as was also
either for the Orussidae or for the Xiphy- concluded by Hoshiba, Matsuura and
driidae, although they are known for Imai (1989). Similarly, available values for
members of two other sawfly families three other parasitoid superfamilies, the
with claims for a close relationship with Diaprioidea (Fig. 5), Scelionoidea and Cy-
the Apocrita, viz the Siricidae and Cephi- nipoidea, are similar. According to Ras-
dae (Konigsmann 1977, Basibuyuk & nitsyn's (1988) phylogenetic hypothesis
Quicke 1994, 1995). In the Cephidae n (see Fig. 4), the Scelionoidea are putatively
ranges from 9 to 22-26 (Mackay 1955, Cro- the sister group of the Chalcidoidea s.l.,
zier and Taschenberg 1972), whilst in the and thus taking the former as the out-
Siricidae, according to Sanderson (1932, group, the plesiomorphic haploid chro-
1970), the haploid number varies between mosome number for the Chalcidoidea
8 and 18. As regards other, less derived maybe postulated asbeing approximately
sawflies, haploid chromosome number 10. Therefore the data collectively support
ranges from 5 to 22 in the Tenthredino- the hypothesis that the small values of n
idea, with three quarters of species having (from 3 to 7) found in the majorityofChal-
an n value rangingbetween 7 and 10 (Nai- cidoidea are likely to be apomorphous.
to 1982). Taking the Siricidae and Cephi- Unfortunately, there are no well founded
dae as the two sawfly families closest to views of relationships within the Chalci-
the ancestral lineage of the Apocrita (i.e. doidea (Trjapitzin 1978, LaSalle 1987, Bou-
putative sister groups of the Apocrita + cek 1988a, Woolley 1988, Noyes 1990, Gib-
Orussidae) for which chromosome num- son 1990), largely perhaps because of the
bers are available, it seems reasonable to considerable plasticity in adult morphol-
conclude that the plesiomorphic haploid ogy displayed by many of the families,
chromosome number in the latter was at which may result because of the undoubt-
least 8 and possibly rather higher. edly polyphyletic natures of some family
Within the Apocrita there is a picture level taxa. Trjapitzin (1978) made few pro-
emerging from independent investiga- posals about higher level relationships,
tions of phylogenetic relationships (Ras- and only suggested two possible group-
nitsyn 1988, Johnson 1988, Gibson 1985, ings, his 'pteromaloid' group comprising
Mason 1983, Quicke et al. 1993, 1994, Her- Pteromalidae, Tanaostigmatidae, Eupel-
aty et al. 1994) that the group divided rel- midae and Encyrtidae, and a 'tetracam-
atively early in its history into a lineage poid' group comprising Tetracampidae,
giving rise to the Ichneumono- Eulophidae, Elasmidae and Aphelinidae.
idea+Aculeata and a second comprising A relationship between the Aphelinidae
