SYSTEMATICS
Phylogenetic Relationships among Subfamilies in Higher Termites
(Isoptera: Termitidae) Based on Mitochondrial COII Gene Sequences
TORU MIURA, KIYOTO MAEKAWA, OSAMU KITADE, TAKUYA ABE,
1
AND TADAO MATSUMOTO
Department of Biology, University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902, Japan
Ann. Entomol. Soc. Am. 91(5): 515-523 (1998)
ABSTRACT Among the 7 families of Isoptera, higher termites (family Termitidae) have acquired
the most complex social systems and widest diversity of feeding habits in the course of adaptive
radiation. Termitidae is composed of 4 subfamilies (Apicotermitinae, Macrotermitinae, Nasutiter-
mitinae, and Termitinae); however, the phylogenetic relationships among subfamilies remains
ambiguous. To test the monophyly of this family and the relationship among the 4 subfamilies, we
sequenced the mitochondrial cytochrome oxidase II (COII) gene in 15 termite genera of Termitidae
and closely related Rhinotermitidae. DNA sequences and translated protein sequences were ana-
lyzed using parsimony and the neighbor-joining method. All the resulting trees gave robust support
for the monophyly of Termitidae, and overall the relationship of Macrotermitinae + (Apicotermiti-
nae + [Termitinae + Nasutitermitinae]) was supported, which is consistent with previous studies
based on morphology.
KEY WORDS Termitidae, molecular phylogeny, mitchondrial DNA, COII gene, relationships
among 4 subfamilies
ONE OF THE major groups of eusocial insects is the
order Isoptera (termites), which is currently recog-
nized as having 7 families and 14 subfamilies (Krishna
1970, Kambhampati et al. 1996). Since the earliest
classification of families, termites have been divided
into 2 major groups: the lower and higher termites
(Snyder 1949, Emerson 1955; reviewed in Krishna
1969). This designation is based mainly on the pres-
ence of symbiotic protozoa in the hindgut of lower
termites. Higher termites consist of only 1 family,
Termitidae, which contains 4 subfamilies—Termiti-
nae, Apicotermitinae, Macrotermitinae, and Nasuti-
termitinae (Krishna 1970, Sands 1972). Termitidae ex-
hibits a wide variety of social specialization and a rigid
caste system with highly stereotyped postembryonic
development (Krishna 1969, Noirot 1969). Moreover,
it is the largest family in Isoptera, containing 3/4 of all
known species. So far, =230 genera have been de-
scribed in Termitidae (Pearce and Waite 1994). Most
of these species are tropical, and abundance is highest
in the area close to the equatorial regions (Collins
1983).
Until the 1970s, the classification of subfamilies dif-
fered from the present one: all genera now in Apico-
termitinae, and some in Termitinae, were classified
into Amitermitinae. It was thought that Amitermitinae
and Termitinae were closely related to each other, and
Macrotermitinae and Nasutitermitinae shared certain
primitive characters (Emerson 1945, Ahmad 1950; re-
1
Center for Ecological Research, Kyoto University, Shimosaka-
moto, Ohtsu, Shiga 520-0105, Japan.
viewed in Krishna 1970). Although Grass6 and Noirot
(1954) erected a new subfamily, Apicotermitinae, it
was not accepted widely. Sands (1972) presented the
phylogeny of higher termites based on intestinal and
mandible morphology. He stressed that Apicotermiti-
nae was an independent subfamily and the rest of
Amitermitinae was included in Termitinae. The gut
morphology of Nasutitermitinae was clearly derived
from Termitinae. Macrotermitinae, with a short intes-
tine like those of the more primitive families of the
lower termites, was distinct from the other 3 subfam-
ilies. Therefore, the inferred relationship was Macro-
termitinae + (Apicotermitinae + [Nasutitermitinae
+ Termitinae]).
Phylogenetic relationships among termite families
has been reported recently, based on mitochondrial
16S ribosomal RNA gene fragment (Kambhampati et
al. 1996). This work showed that Mastotermitidae was
the most basal taxon in termites, and Termopsidae was
more basal than Kalotermitidae, which was the sister
taxon of the Rhinotermitidae-Termitidae complex. In
the study, however, the monophyly of Termitidae was
not supported strongly. In addition, the relationships
among subfamilies in higher termites (Termitidae)
has not been examined based on molecular data.
In this study we sequenced the mitochondrial cy-
tochrome oxidase II (COII) gene and analyzed the
phylogenetic relationship using neighbor-joining and
most-parsimony method, in order to clarify the mono-
phyly of Termitidae and the relationships among the
four subfamilies of higher termites.
0013-8746/98/0515-0523302.00/0 © 1998 Entomological Society of America
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