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ANRV297-EN52-08 ARI 21 November 2006 10:19
Evolutionary Biology of
Centipedes (Myriapoda:
Chilopoda)
Gregory D. Edgecombe
1
and Gonzalo Giribet
2
1
Australian Museum, Sydney, New South Wales 2010, Australia;
email: greged@austmust.gov.au
2
Department of Organismic & Evolutionary Biology and Museum of Comparative
Zoology, Harvard University, Cambridge, Massachusetts 02138;
email: ggiribet@oeb.harvard.edu
Annu. Rev. Entomol. 2007. 52:151–70
First published online as a Review in
Advance on July 27, 2006
The Annual Review of Entomology is online at
ento.annualreviews.org
This article’s doi:
10.1146/annurev.ento.52.110405.091326
Copyright
c
2007 by Annual Reviews.
All rights reserved
0066-4170/07/0107-0151$20.00
Key Words
arthropod phylogeny, biogeography, evodevo
Abstract
New insights into the anatomy, systematics, and biogeography of
centipedes have put these predatory terrestrial arthropods at the
forefront of evolutionary studies. Centipedes have also played a piv-
otal role in understanding high-level arthropod relationships. Their
deep evolutionary history, with a fossil record spanning 420 million
years, explains their current worldwide distribution. Recent analy-
ses of combined morphological and molecular data provide a stable
phylogeny that underpins evolutionary interpretations of their bi-
ology. The centipede trunk, with its first pair of legs modified into
a venom-delivering organ followed by 15 to 191 leg pairs, is a fo-
cus of arthropod segmentation studies. Gene expression studies and
phylogenetics shed light on key questions in evolutionary develop-
mental biology concerning the often group-specific fixed number of
trunk segments, how some centipedes add segments after hatching
whereas others hatch with the complete segment count, the addi-
tion of segments through evolution, and the invariably odd number
of leg-bearing trunk segments.
151
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Segmentation:
serial repetition of
body structures
along the
anterior-posterior
body axis
Gene expression:
the spatial and
temporal
deployment of gene
products
INTRODUCTION
Centipedes (Chilopoda)—one of the four ma-
jor lineages of myriapods—are an important
group of predatory arthropods in many terres-
trial habitats. They comprise approximately
3300 species belonging to the five extant or-
ders illustrated in Figure 1, and one extinct
order represented by a single species (84).
Centipedes are known from all continents ex-
cept Antarctica, with the greatest diversity
occurring in the tropics and warm temper-
ate regions, and have a fossil record spanning
420 million years. Most species inhabit leaf
litter and soil or are found under stones, bark,
or wood in forests, although grassland, desert,
caves, and the littoral zone are occupied by
some species.
Centipedes are typically solitary except
when brooding their eggs or hatchlings. Adult
body length ranges from 4 to 300 mm, with
most species measuring 10 to 100 mm long.
They are almost exclusively predatory and,
commensurate with their size range, in most
cases feed on small live arthropods and other
invertebrates, although large scolopendrids
can take vertebrate prey (67). The prey is im-
mobilized by venom injected from the poison
glands, which are housed in a modified first
pair of trunk legs (63). In all centipedes these
legs are functionally incorporated into the
head as a pair of maxillipedes (also called for-
cipulae), this modified pair of appendages be-
ing the most conspicuous shared derived char-
acter of Chilopoda. The majority of species
are nocturnal, and they live most of their lives
cryptically.
Centipedes have fascinated all kinds of
biologists, including ecologists interested in
their modes of life and biodiversity, biogeog-
raphers interested in understanding their cur-
rent and past distributions, and systematists
interested in the pivotal role of centipedes
in understanding arthropod phylogeny. Evo-
lutionary developmental biologists use cen-
tipedes as models to understand segmentation
because of the uniqueness of the myriapod
body plan based on its serial repetition of seg-
ments. In addition, centipedes are of medical
importance owing to the presence of powerful
neurotoxic venoms (11).
Aside from taxonomy and systematics,
some of the most interesting topics in cen-
tipede evolution are the modes of develop-
ment and the number of trunk segments,
as well as the different modes of maternal
care displayed by some centipede groups. The
study of these characters and trends requires
a sound understanding of centipede relation-
ships. The typical centipede body plan in-
cludes six head segments followed by the pair
of maxillipedes, a series of trunk leg-bearing
segments with one pair of legs per segment,
and two genital segments. The number of
leg-bearing trunk segments (pairs of walking
legs) varies between groups (Table 1). Sev-
eral groups have 15 leg-bearing trunk seg-
ments, while some have up to 191 pairs of
legs. Intermediate states with 21 and 23 pairs
of legs occur in the scolopendromorphs, and
in geophilomorphs the number of leg-bearing
segments ranges from 27 to the aforemen-
tioned 191. Interestingly, this is always an
odd number, so the number of trunk seg-
ments (including the maxillipede segment) is
always even. The raw number of segments in
each species can be fixed or it can vary within
the different orders (Table 1). The number
of leg pairs is conserved in the members of
the orders Scutigeromorpha, Lithobiomor-
pha, and Craterostigmomorpha, whereas it
varies slightly in Scolopendromorpha and
enormously in Geophilomorpha. The num-
ber of segments has relevance to the develop-
ment of models for segmentation, both within
centipedes and in arthropods, questions that
have recently received attention from the per-
spective of gene expression data in embryos
(13, 45).
The addition of segments through de-
velopment is another key question in cen-
tipede evolution, because some groups hatch
with the complete adult number of segments
(epimorphosis), whereas others add segments
after hatching (anamorphosis) (see Sidebar).
Whether epimorphosis or anamorphosis is
152 Edgecombe
·
Giribet
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Figure 1
Life images of the five extant centipede orders. (a) Scutigeromorpha: Parascutigera sp., a scutigerid from
Lane Poole Reserve (Western Australia). (b) Lithobiomorpha: Cermatobius japonicus, a henicopid from
Mount Takao (Japan). (c) Craterostigmomorpha: Craterostigmus cf. tasmanianus from Mount Cook/Aoraki
National Park (New Zealand). (d ) Scolopendromorpha: Cormocephalus aurantiipes, a scolopendrid from
Lane Poole Reserve (Western Australia). (e) Scolopendromorpha: Cormocephalus hartmeyeri from
Porongurup National Park (Western Australia) brooding peripatoid stage hatchlings. ( f )
Geophilomorpha: Zelanophilus provocator, a geophilid from Hinewai Scenic Reserve (New Zealand).
Photographs by the authors.
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Evolutionary Biology of Centipedes 153
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Table 1 Number of adult and hatchling leg-bearing trunk
segments and mode of development
Adult Hatchling Development
Scutigeromorpha 15 4 Anamorphic
Lithobiomorpha 15 6–8 (7)
a
Anamorphic
Craterostigmomorpha 15 12 Anamorphic
Scolopendromorpha 21–23 21–23 Epimorphic
Scolopocryptopidae 23 23 Epimorphic
Others 21 21 Epimorphic
Geophilomorpha 27–191 27–191 Epimorphic
Mecistocephalidae 47–101 47–101 Epimorphic
Adesmata 27–191 27–191 Epimorphic
a
Value in parenthesis indicates most common number of hatchling
leg-bearing trunk segments.
the primitive condition in centipedes has been
extensively debated in the literature, but only
through a rigorous phylogenetic framework
can we understand this important evolution-
ary trend. Finally, some centipedes display
maternal brood care, although whether the
mother guards the brood with her sternal
(ventral) or tergal (dorsal) regions is also of
evolutionary significance.
In this article we review these important
aspects of centipede evolutionary biology and
MODES OF SEGMENT ADDITION
Being multisegmented, arthropods need to develop a series
of segments often of functional equivalence. They develop in
two radically different ways. Some species hatch with a final
number of segments, as occurs in all insects and in scolopen-
dromorph and geophilomorph centipedes. This mode of de-
velopment is known as epimorphosis. On the contrary, in
anamorphosis segments are added throughout postembryonic
development. Three main modes of anamorphic development
are recognized (31). In euanamorphosis segments are added
throughout the entire life of the animal, as occurs in some
long-bodied millipedes. In teloanamorphosis segments are
added until a final stage, with no further molting, as is the
case for polydesmid millipedes. Finally, in hemianamorpho-
sis molting continues after the final number of segments has
been reached. The latter is the type of anamorphic develop-
ment that occurs in the nonepimorph centipedes.
place them in a phylogenetic context. We also
revise the most current interpretations of the
position of centipedes within the arthropod
tree of life and focus on relationships be-
tween centipede orders, a topic that has re-
ceived enormous attention from detailed mor-
phoanatomical studies and their combination
with multiple sources of molecular data. The
intention of this review is to further the cur-
rent understanding of this fascinating and an-
cient group of terrestrial arthropods, which
plays a major role as predators in most terres-
trial ecosystems.
CENTIPEDES AND
ARTHROPOD PHYLOGENY
Myriapod Monophyly?
The position of centipedes in the arthro-
pod tree of life is tied to a question con-
cerning the monophyly of Myriapoda. In
addition to Chilopoda, Myriapoda includes
three other groups: Symphyla, Pauropoda,
and Diplopoda. Symphylans and pauropods
are relatively minor groups, known from only
200 and 700 species (1), respectively, whereas
Diplopoda (millipedes) includes 11,000 de-
scribed species (1). Pauropods and diplopods
are nearly universally recognized as each
others’ closest relatives, together forming
the clade Dignatha, and most morphologists
identify Symphyla as their sister group (16, 23,
54). Collectively these three myriapod classes
comprise the clade Progoneata, named for the
positioning of the genital opening anteriorly
on the trunk, behind the second pair of legs—
in contrast, Chilopoda are opisthogoneate,
with the genital opening located terminally
on the body, as in insects. The fundamen-
tal question over Myriapoda is then whether
centipedes are part of a natural group with the
progoneate myriapods (16). Recent studies us-
ing either morphology or molecular data have
variably resolved myriapods as monophyletic
(23, 36, 37, 79, 80), paraphyletic (53, 55, 71),
or polyphyletic (57), although the case for
monophyly is sustained by the largest amount
of evidence.
154 Edgecombe
·
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Morphological arguments in favor of the
monophyly of Myriapoda are principally de-
rived from the structure and movements of the
cephalic tentorial endoskeleton and the struc-
ture of the mandibles (23). The classic argu-
ment for myriapod monophyly is the abduc-
tion of the mandibles by the movements of the
anterior tentorial arms, the so-called swinging
tentorium (60). The tentorium of Chilopoda
and Progoneata shares a common pattern of
fusion of its posterior process to a trans-
verse bar that extends to the lateral cranial
wall (7, 52). Myriapod mandibles are struc-
turally unique in that they are divided into a
movable, independently musculated gnathal
lobe and a base plate. The separation of the
gnathal lobe is marked by a large flexor muscle
with a common point of origin on the cranial
roof.
Mandibulata
For most of the past century, most morphol-
ogists have united myriapods with hexapods
and crustaceans on the basis of the shared
presence of mandibles as the anterior-most
adult mouthpart, formed from the appendages
of the post-tritocerebral segment. This clade
has been named Mandibulata. Mandibles are
embedded in a chewing chamber in the head
capsule; their musculature indicates a com-
mon identity as a coxal gnathobase, and
they share similar substructures on their bit-
ing edge (30). Classical morphological ar-
guments for the homology of mandibles
have been strengthened by gene expression
data. For example, mandibles are differenti-
ated from other appendages in their gradient
of decreasing expression of the homeobox-
containing gene distal-less through ontogeny
(74, 82); the expression pattern of this gene
as well as dachshund (75) reinforces the uni-
formly gnathobasic identity of mandibles.
In addition to the mandible itself, mono-
phyly of Mandibulata finds support from the
ultrastructure of the compound eyes, no-
tably the presence of a crystalline cone com-
posed of four cone cells, primary pigment
Mandible: first
appendage
innervated by a
ganglion located
behind the brain,
transformed for
chewing in
myriapods,
crustaceans, and
insects
Hox genes: a family
of homeodomain
transcription factors
generated by tandem
duplication that
specify position
along the
anterior-posterior
axis of the animal
cells, and interommatidial pigment cells that
are found in scutigeromorph centipedes as
well as in crustaceans and hexapods (69).
Other evidence for a natural grouping of
Mandibulata includes the expression patterns
of Hox genes in the head [(45, 46); data
for Chilopoda based on Lithobius atkinsoni],
specific serotonin-immunoreactive neurons
[(39); data for Chilopoda based on L. forfi-
catus and Scolopendra sp.], the organization of
the brain neuropils (40), and hemocyanin se-
quence data (56).
In the context of the Mandibulata hy-
pothesis, myriapods have traditionally been
united with hexapods to form a group named
Atelocerata or Tracheata (54). The Atelo-
cerata hypothesis has been seriously chal-
lenged by the analysis of molecular data, many
kinds of which instead suggest a crustacean-
hexapod grouping. These include sequence
data for nuclear ribosomal genes (58), nu-
clear coding genes (79), mitochondrial genes
(48), Hox genes (15), hemocyanin (56), or
the combination of multiple loci and mor-
phology (36, 37). Morphological support
for a crustacean-hexapod clade includes sev-
eral neurological characters, including brain
structure (87), generation of ganglion mother
cells by the mitotic division of neuroblasts
(40), and specific early-differentiating neu-
rons (20) and pairs of serotonergic neurons
(39).
If hexapods are most closely related to—
or derived from—crustaceans, as favored by
virtually all kinds of molecular data and a
suite of neurological characters, then there
is little question that myriapods are mono-
phyletic because the atelocerate characters
[such as a limbless intercalary (tritocerebral)
segment in the head, the ectodermally derived
Malpighian tubules, and a cuticular cephalic
tentorial endoskeleton] would serve as addi-
tional myriapod characters.
Paradoxopoda
A closer relationship between myriapods and
chelicerates than either shares with hexapods
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Tardigrada
Onychophora
Pycnogonida
Chelicerata
Chilopoda
Diplopoda
Symphyla
Pauropoda
Hexapoda
‘Crustacea’
Myriapoda
Tetraconata
Arthropoda
Mandibulata
Figure 2
Schematic tree of the interrelationships of the major arthropod groups, illustrating the position of
Chilopoda and Myriapoda. This tree is based mostly on References 23 and 37.
or crustaceans has been found in some molec-
ular studies, including analyses of nuclear ri-
bosomal genes (58) as well as mitochondrial
genes (48, 71, 73) and Hox genes (15). The
myriapod-chelicerate group has been named
Paradoxopoda (58) or Myriochelata (73) and
has never been previously proposed on the ba-
sis of anatomical data.
The Paradoxopoda hypothesis conflicts
with the substantial body of morphological
support for Mandibulata and is itself with-
out compelling morphological support. To
date, the only suggestion for a myriapod-
chelicerate group from the perspective of
morphology is derived from a shared pattern
of neurogenesis in a spider, a millipede, and a
lithobiomorph centipede (19, 49). In each of
these arthropods, the neural precursors form
similar groups of cells that invaginate from the
neuroectoderm. It cannot be ruled out that
the myriapod-chelicerate pattern of neuroge-
nesis is simply plesiomorphic for arthropods,
in contrast to the shared role of neuroblasts
in generating the neuronal precursor cells in
crustaceans and hexapods (40).
The most comprehensively sampled analy-
sis of combined morphological and molecular
sequence data (37) support the monophyly of
Mandibulata over more analytical conditions
that support the Paradoxopoda hypothesis (14
versus 2), including the conditions that max-
imize overall congruence among all data. A
crustacean-hexapod clade, Tetraconata, is also
stable to analytical variation, and Myriapoda is
monophyletic under most analytical regimes
(Figure 2).
MORPHOLOGY, MOLECULES,
AND SYSTEMATICS OF THE
FIVE EXTANT CENTIPEDE
ORDERS
Extant centipedes are grouped in five orders,
all of which are currently recognized as mono-
phyletic entities. In this section we discuss
each of these orders and provide the evi-
dence that has been used to support their
monophyly.
Scutigeromorpha
Scutigeromorpha (Figure 1a) consists of 100
valid species (∼200 named species) assigned
to three families: Pselliodidae, Scutigeri-
dae, and Scutigerinidae. The most famil-
iar and best-studied species is Scutigera
156 Edgecombe
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Figure 3
External morphological characters distinguishing Notostigmophora (a, e, Scutigera coleoptrata; c,
Thereuonema tuberculata) and Pleurostigmophora (b, d, f, Lithobius obscurus). (a) Domed head capsule,
showing antennae (ant), compound eye (c.e), maxillipede (mxpd), and second maxillae (mx2). (b)
Flattened head capsule, with cluster of ocelli (oc); other abbreviations as in a.(c) Maxillipedes, with
flexible hinge between coxae indicated by arrow. (d ) Maxillipedes, with coxae joined (arrow). (e) Head (at
right) and first two tergal plates, showing spiracles (sp) opening dorsally. ( f ) Tergal plates 3–5, showing
spiracles (sp) opening above leg bases. Scanning electron micrographs by Sue Lindsay (Australian
Museum). Scale: 0.25 mm.
coleoptrata, a circum-Mediterranean native
that is the synanthropic house centipede in
many other parts of the world. The mono-
phyly of Scutigeromorpha is amply supported
by numerous unique characters (27). The
antennae are multiannulated flagella usually
composed of a few hundred ring-like articles
(Figure 3a). The respiratory system features
tracheal lungs opening to a spiracle on the
posterior part of the tergites (Figure 3e)—
in all other chilopods the spiracles open
above the leg bases, at the sides of the body
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(Figure 3f ). Scutigeromorphs are the only
centipedes that use hemocyanin as the oxy-
gen transport molecule (59). Eight elon-
gate tergal plates cover the 15 pairs of
trunk legs. Scutigeromorphs have faceted eyes
(Figure 3a), the ultrastructure of which cor-
responds to ommatidia of the compound eyes
of crustaceans and hexapods (69). The head
contains several distinctive organs and glands
(44).
Scutigeromorphs are remarkably fleet-
footed, running at speeds of up to 40 cm s
−1
(61). Mothers lay single eggs, which are aban-
doned in the soil. Hatchlings have four pairs
of legs and are active; the remaining segments
are added through a series of molts.
Lithobiomorpha
The order Lithobiomorpha (Figure 1b)
includes 1100 valid species among more than
1800 named species. Its most familiar species
is the common European and North Ameri-
can Lithobius forficatus. Two families are recog-
nized, one principally Laurasian (Lithobiidae)
and the other principally Gondwanan
(Henicopidae). Lithobiomorpha is the only
centipede order whose monophyly has
been questioned, but ample evidence from
morphology and molecular sequence data has
accumulated in recent studies to defend the
group’s monophyly (22, 25).
Lithobiomorphs are rarely more than
30 mm long and have 15 pairs of trunk legs.
The head shield is flattened, with either a
cluster of ocelli on each side of the head
(in Lithobiidae) (Figure 3b) or a single ocel-
lus on each side of the head (in Henicopidae).
The antenna consists of 15 to more than 100
articles. The trunk has long tergites on leg-
bearing segments 1, 3, 5, 7, 8, 10, 12, and 14
and short tergites on the alternating segments.
Postembryonic development is anamorphic,
as in scutigeromorphs, and eggs are likewise
laid singly without maternal care. Hatchlings
usually have seven (although in some species
six or eight) leg pairs. Characters that unite
Lithobiomorpha as a monophyletic group in-
clude plumose setae on the second maxillary
tarsus, a transverse seta that projects medially
from the labral sidepiece, and a female gono-
pod with its basal article bearing macrosetae
(spurs) and having a broad claw.
Craterostigmomorpha
Craterostigmus tasmanianus is the sole de-
scribed species of the order Craterostig-
momorpha. Originally known from and
widespread throughout the Australian state of
Tasmania, Craterostigmus also occurs through-
out New Zealand (Figure 1c). The New
Zealand collections are morphologically in-
distinct from C. tasmanianus. Unique charac-
ters of Craterostigmus include subdivision of
the long tergites so that the trunk appears to
have 21 tergites covering the 15 pairs of trunk
legs; long maxillipedes, projecting in front of
the head plate; sclerites of the fifteenth leg-
bearing segment fused as a complete cylindri-
cal ring; and the anogenital region enclosed
in a bivalved capsule that opens ventrally to
expose a meshwork of openings for the coxal
organs.
Because of its isolated systematic position,
the morphology, ultrastructure, and genetics
of C. tasmanianus have been investigated in de-
tail. Important contributions have been made
on external morphology and internal anatomy
(10, 18, 61), together with detailed studies of
the genital systems (78), spermatophore and
sperm ultrastructure (12), anal organs (81),
tracheae (42), eyes (68a), and the circulatory
system (91).
Scolopendromorpha
The order Scolopendromorpha (Figure 1d,e)
is the most aggressive and most voracious
predators among the centipedes, with body
length reaching up to 30 cm in the Neotrop-
ical Scolopendra gigantea. More than 800 valid
species (from nearly 1300 named species) are
known, generally classified into three fami-
lies on the basis of leg count and the presence
or absence of a cluster of four lateral ocelli.
158 Edgecombe
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Scolopendrids and cryptopids have 21 pairs
of trunk legs, whereas scolopocryptopids have
23 pairs.
Unique characters that define Scolopen-
dromorpha include a single tergite covering
both the maxillipede segment and the first leg-
bearing trunk segment; the spiracles served
by muscles that have an apodemal function
(42); a bean-shaped spermatophore with a
tough, multilayered wall; and a rudimentary
left oviduct and ejaculatory duct (77).
Scolopendromorphs share important as-
pects of their embryology and early postem-
bryonic development with Geophilomorpha.
Both have epimorphic development and the
mother broods the eggs and two nonfeeding
posthatching stages.
Geophilomorpha
Geophilomorpha (Figure 1f ) is by far the
most diverse centipede order at the familial
level, with 14 families currently recognized
to accommodate approximately 1300 valid
species among more than 1700 named species.
Derived characters shared by all geophilo-
morphs include the nearly homonomous
trunk segments with a spiracle on all leg-
bearing trunk segments except the last, and a
greater number of segments than in other cen-
tipedes. Geophilomorphs differ from other
chilopods in that the number of trunk seg-
ments is usually variable within a species
[sometimes greatly so, e.g., 87 to 177 seg-
ments in Himantarium gabrielis (2)], despite
the fact that no segments are added after
hatching, with females usually having more
segments than males. All species are blind,
and the brain has a less clear differentiation
of its three lobes compared with the other
chilopods. The antennal segment number is
precisely fixed at 14 segments. The trunk ter-
gites are divided into prominent pretergites
and metatergites, each independently muscu-
lated, a feature that has been linked to the bur-
rowing habits of these centipedes (61).
A compelling suite of morphological, be-
havioral, and molecular characters divides
Geophilomorpha into the clades Placodes-
mata (composed of a single family, Mecisto-
cephalidae) and Adesmata (all other families).
Mecistocephalids are the only geophilo-
morphs in which mothers brood with the
sternum against the eggs or hatchlings, as is
also the case in scolopendromorphs (9). All
other geophilomorphs brood with the ster-
num upward. This behavioral shift is asso-
ciated with a significant morphological in-
novation; in Adesmata, defensive glands are
developed along the trunk, and the brood-
ing ritual has evidently been modified to keep
the noxious defensive secretions out of con-
tact from the brood (9). An additional argu-
ment for a basal position of mecistocephalids
within Geophilomorpha is the fixed numbers
of segments within species (without sexual di-
morphism), as in all other centipede orders.
EVOLUTIONARY
RELATIONSHIPS BETWEEN
THE CENTIPEDE ORDERS
Of all major arthropod groups, Chilopoda
is perhaps the clade with the most uni-
versal consensus on the pattern of higher-
level phylogenetic relationships (Figure 4),
at least from the perspective of morphol-
ogy. Molecular sequence data, especially se-
quences from nuclear ribosomal genes, have
generally reinforced relationships based on
morphology (33). The most substantial incon-
gruence is found between different molecular
markers rather than between molecules and
morphology (34).
The first Hennigian analysis of rela-
tionships between the five extant orders
of centipedes (17) endorsed a basal divi-
sion of Chilopoda into Notostigmophora
( = Scutigeromorpha) and Pleurostigmo-
phora that had been proposed in precladistic
times. More recent analyses have been based
on datasets that sample chilopod diversity us-
ing a large number of exemplar species rather
than ordinal ground patterns, coding for the
same set of species as were used in molecular
analyses (25, 28). These analyses support the
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Pselliodidae
Scutigerinidae
Scutigeridae
Lithobiidae
Henicopidae
Craterostigmidae
Devonobiidae
Scutigeromorpha
Lithobiomorpha
Craterostigmomorpha
Devonobiomorpha
Pleurostigmophora
Phylactometria
Epimorpha
Notostigmophora
Scolopendridae
Cryptopidae
Mecistocephalidae
Neogeophilidae
Macronicophilidae
Eucratonychidae
Eriphantidae
Gonibregmatidae
Oryidae
Linothaeniidae
Aphilodontidae
Dignathodontidae
Geophilidae
Ballophilidae
Schendylidae
Himantariidae
Scolopendromorpha
Geophilomorpha
Adesmata
Scolopocryptopidae
Figure 4
Summary tree of the relationships among centipede families. This tree is based mostly on data provided
in Reference 25; geophilomorph relationships are based on data provided in Reference 32.
Notostigmophora-Pleurostigmophora split
that has also been recognized by studies based
on either non-numerical cladistic analysis
(84, 86) or studies of particular character
systems (81, 91). Pleurostigmophora is
supported by such apomorphic characters as
the flattening of the head plate (Figure 3b),
medial coalescence of the maxillipede coxae
(Figure 3d ), a maxillipede tarsungulum
(fused tarsus and pretarsus), pleural spiracles
(Figure 3f ), coxal organs, spermatophore
deposition on a web, and ultrastructure of the
lateral ocelli (68, 68a).
Acceptance of the Pleurostigmophora
concept means that the division of Chilopoda
into Anamorpha and Epimorpha (4) on the ba-
sis of anamorphic versus epimorphic develop-
ment is unwarranted. Anamorphosis is instead
resolved as a plesiomorphic character shared
between Scutigeromorpha, Lithobiomorpha,
and Craterostigmomorpha, the last reducing
the anamorphic phase to a single instar with 12
leg pairs. Epimorphosis maps onto the clado-
gram as a synapomorphy for Scolopendro-
morpha + Geophilomorpha, a clade named
Epimorpha (Figure 4).
Other morphogenetic characters are cor-
related with the difference between anamor-
phic and epimorphic development. The two
orders with prolonged anamorphic phases
160 Edgecombe
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regenerate legs after loss, whereas in the epi-
morphic orders regeneration happens for the
last legs only or not at all (66). Geophilo-
morphs, which have the lowest number of an-
tennal segments, are unique in not adding an-
tennal segments after hatching and in lacking
the capacity to regenerate antennae (66).
Most morphological and combined mor-
phological and molecular analyses unite
Craterostigmomorpha with Epimorpha. This
group shares maternal care of the eggs and
hatchlings and has been named Phylactome-
tria for this behavior (25). Other diagnostic
characters include a strengthening of the max-
illipedes, with the hinge between the coxos-
ternites fused, and the testes having lateral
vesicles (76).
A topology conflicting with the morpho-
logical cladogram is produced by analyses
of three nuclear coding genes (80). These
data resolve Craterostigmus as sister to all
other chilopods and support a sister group
relationship between Scutigeromorpha and
Scolopendromorpha. When these data are
combined with four other genes and morphol-
ogy, two basic tree topologies are obtained
(34). The classical topology emerges under
certain parameter sets in which the riboso-
mal genes represent a larger portion of the
total cladogram length, while under the com-
plementary parameter sets the topology ob-
tained from the nuclear protein-coding genes
dominates.
BIOGEOGRAPHY AND
CENTIPEDES
Many groups of centipedes have relatively
narrow geographic distributions. Low in-
dividual vagility and restricted geographic
distributions of species render these taxa
useful subjects for historical biogeographic
studies. Exceptions to narrow-range en-
demism are known within each of the major
groups. Among the most widespread dis-
tributions, each known from several conti-
nents across a range of climatic zones, are
Pachymerium ferrugineum (Geophilomorpha),
Lamyctes emarginatus (Lithobiomorpha), and
Scutigera coleoptrata (Scutigeromorpha). P. fer-
rugineum is highly resistant to immersion in
water, which may account for its occurrence
on far-flung islands. L. emarginatus repro-
duces by parthenogenesis throughout most
of its range, a strategy that has facilitated
its nearly cosmopolitan distribution. S. coleop-
trata is synanthropic through much of its
range, as described above, and although it is
identified as a single morphospecies, it ex-
hibits substantial genetic variation (27).
The three families of Scutigeromorpha
have largely disjunct distributions, and two
of them are restricted to only two continen-
tal fragments (Figure 5). Scutigerinidae is
endemic to southern Africa and Madagascar
and Pselliodidae is restricted to the Neotrop-
ics and tropical Africa. Scutigeridae is the
most widespread family, including all of the
scutigeromorphs in Europe, North Africa,
Asia, Australia, and the Pacific Islands.
In Lithobiomorpha, the mostly Southern
Hemisphere family Henicopidae has been
subjected to cladistic analyses that pro-
vide a framework for biogeographic analy-
ses (24, 29). The most persistent problems in
the higher-level systematics of Henicopidae
involve groups with disjunct biogeographic
distributions (24). The small, blind Anop-
sobiinae are resolved as sister to all other
Henicopidae in most analyses. Within this
group, most species diversity belongs to a
well-defined Gondwanan clade, with mem-
bers in Australia, New Zealand, New Cale-
donia, southern South America, and southern
Africa (26). Five monotypic genera of Anop-
sobiinae have widely separated occurrences in
the Northern Hemisphere, including Japan,
Tajikistan, the island of Rhodes (likely a
synanthropic introduction), and Kazakhstan.
The henicopine tribe Zygethobiini has
likewise proved to be of uncertain monophyly
(24) and involves a disjunct trans-Pacific dis-
tribution. Its members include two or three
Nearctic genera and two Oriental genera. The
trans-Pacific distribution of Zygethobiini is
largely congruent with that of the lithobiid
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Figure 5
Exemplar taxon distributions for Scutigerinidae, Pselliodidae, and Bothropolys.
Gondwana:
southern
supercontinent
including the present
Africa, Antarctica,
Australia, India,
Madagascar, and
South America that
began rifting apart in
the Jurassic period
genus Bothropolys (21), which is found in East
and Southeast Asia and in North America
(Figure 5).
The most comprehensive phylogenetic
and biogeographic data are available for
the predominantly southern temperate
Henicopini. The genus Paralamyctes has been
used for biogeographic analyses because
of its endemicity to most major fragments
of Gondwana, including southern Africa,
Madagascar, India, Patagonia, eastern
Australia, and New Zealand. A cladogram for
Paralamyctes has been constructed using 20 of
the 26 known species of the genus (35). The
phylogenetic analysis identified two main
clades: One unites species from southern
Africa, Madagascar, tropical to subtropical
Australia, and New Zealand, and the other
includes species found in temperate Australia,
New Zealand, and Chile. The biogeographic
analysis concluded that Australian clades
have closest affinities to other Gondwanan
fragments.
The disjunct populations of Craterostig-
mus in Tasmania and in New Zealand pose
a biogeographic enigma because no mor-
phological differentiation has been found
between them. However, genetic differen-
tiation in mitochondrial genes is substan-
tial (25). Analysis of 16S rRNA shows lev-
els of divergence similar to those among
different species of lithobiomorphs and
scolopendromorphs.
A detailed morphological cladistic analysis
of the geophilomorph family Mecistocephal-
idae suggests an evolutionary trend toward
an increase in segment number (8). Certain
groups have highly disjunct biogeographic
distributions (e.g., Dicellophilus in central Eu-
rope, Japan, and California) that may suggest
that the current distribution is a relict of a for-
merly more widespread condition. Similarly,
a revision of the Neotropical geophilomorph
taxa suggests that certain clades preserve re-
lictual Gondwanan distributions, although
the majority of the biota has a cosmopolitan
distribution that originated through more re-
cent dispersal (72).
Because of their typical variation in seg-
ment numbers within a species, adesmatan
geophilomorphs can be examined from the
perspective of geographic variation in seg-
mentation. Latitudinal clines in segment
numbers have been documented in several
species in Britain (3, 50), indicating an in-
crease in the number of segments in more
162 Edgecombe
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southerly populations compared with their
more northerly conspecifics.
CENTIPEDES AND THE FOSSIL
RECORD
Because centipedes have an unmineralized ex-
oskeleton and generally inhabit nonaquatic
sites with low fossilization potential, their fos-
sil record is patchy. Even so, their history
extends back to the latest Silurian, approx-
imately 418 Mya. Each of the four diverse
centipede orders is known from amber fos-
sils, and of these only Lithobiomorpha lacks a
pre-Cenozoic fossil record. As is the case for
myriapods in general, geologically early cen-
tipede fossils are surprisingly modern and can
be identified as members of the crown-group
of Chilopoda (84, 85).
The earliest known fossil centipedes can
be confidently assigned to Scutigeromorpha.
The Silurian-Devonian genus Crussolum (1a,
85) has the pentagonal cross-section of the
leg podomeres with rows of sawblade-like
spines that are retained in extant scutigero-
morphs. The maxillipede has a separation be-
tween the coxosternites and robust spine bris-
tles along the margin of the coxosternum, as
in extant Scutigeromorpha (1a). Crussolum is
known from the latest Silurian in England, the
Lower Devonian of Scotland, and the Middle
Devonian of Gilboa, New York. Other fos-
sil scutigeromorphs include the Upper Car-
boniferous Latzelia, from the Mazon Creek
deposits of Illinois (70), and the Lower Cre-
taceous Fulmenocursor, from the Crato Forma-
tion in northeastern Brazil (89). Fulmenocursor
has short antennal articles and style-like male
gonopods that suggest membership in the ex-
tant family Scutigeridae.
Devonobius delta, from the Middle
Devonian of Gilboa, New York, is a repre-
sentative of the monotypic order Devono-
biomorpha and is known from magnificently
preserved cuticular remains (84). The head
and anterior part of the trunk are preserved,
but the complete number of segments (at least
16) is unknown. Its most distinctive character
is the presence of long ventral apodemes on
the maxillipede that are unknown in extant
chilopods. Devonobius was initially interpreted
as the sister group of Epimorpha (84) but
was subsequently regarded as most closely
related to Craterostigmus (10). The characters
cited in support of this latter relationship do
not withstand scrutiny (25), and parsimony
analysis of morphology leaves the position
of Devonobius unresolved with respect to
Craterostigmus and Epimorpha.
Paleozoic scolopendromorphs are known
exclusively from two species in the Upper Car-
boniferous deposits of Mazon Creek, Illinois.
The better known, Mazoscolopendra richardsoni
(70), has 21 leg-bearing trunk segments as in
Scolopendridae and Cryptopidae. The Meso-
zoic record of scolopendromorphs is based
on two species from the Lower Cretaceous
of northeastern Brazil, Velocipede betimari and
Cratoraricrus oberlii (62, 90). The latter is the
better understood of the two, possessing some
characters typical of Scolopendridae (90).
The earliest reasonably established
geophilomorph is Eogeophilus jurassicus, from
the Upper Jurassic Solnhofen limestones of
Germany (83). Although the habitus of this
species is unquestionably geophilomorph, it
presents a puzzling incongruence in the form
of the maxillipedes. Extant geophilomorphs
share a joint between the first and fourth
articles of the telopodite. This modification
is shared with scolopendromorphs and
has been regarded as a synapomorphy for
Scolopendromorpha and Geophilomorpha.
Eogeophilus has complete (unreduced) second
and third articles. Interpreting the form
of Eogeophilus to be plesiomorphic forces a
convergence between extant geophilomorphs
and scolopendromorphs.
CENTIPEDES AND
EVOLUTIONARY
DEVELOPMENTAL BIOLOGY
Two important aspects of centipedes are cur-
rently at the forefront of evolutionary and
developmental biology studies—the patterns
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Tagmosis: type of
segmentation in
which groups of
segments acquire a
specific function and
delimit different
body regions
and modes of segmentation. The addition
of segments through evolution is an impor-
tant theme in the group. The fixed number
of trunk segments in most centipede species
and the switch from an anamorphic devel-
opmental mode to an epimorphic one in the
course of centipede phylogeny—including an
intermediate stage in Craterostigmus—have
captivated evolutionary developmental biolo-
gists interested in the evolution of segmenta-
tion in arthropods in general and in myriapods
in particular.
One of the peculiarities of centipede seg-
mentation is the invariant odd number of
leg-bearing trunk segments. The basis of this
developmental constraint on pairing of seg-
ments that leads to an odd segment num-
ber has been elucidated in Strigamia mar-
itima, which is also the only exception to
the rule, with a mutant having 48 pairs of
legs (produced by a duplication of the ulti-
mate leg-bearing segment) (51). Recent em-
bryological studies of this species, including
expression data for segmentation genes (14),
have corrected a fundamental error in the de-
scription of the anterior-posterior body axis in
centipede embryos introduced by Heymons
(41) and widely perpetuated in subsequent
literature. The corrected description recog-
nizes segmentation originating in a termi-
nal growth zone, with rings of expression of
segmentation genes around the proctodeum
that fade anteriorly. Expression bands for odd-
skipped and caudal show that the odd trunk seg-
ment number arises via a double-segmental
pair-rule patterning involving two phases of
segmentation (13). Intriguingly, the double
phase of segmentation described for S. mar-
itima was not detected in Lithobius atkin-
soni, for which segmentation genes indicate
a strictly one-by-one formation of segments
(45).
Variation in numbers of trunk segments
in centipedes has been explored using a
meromeric model of segmentation (64). The
model implies a trunk originally consisting
of eight primary units called eosegments,
each of which subsequently divided into sec-
ondary units known as merosegments. The
16-segment trunk—maxillipede plus the 15
leg-bearing segments—would thus be gener-
ated by a single phase of meromeric duplica-
tion of the original eight eosegments. Addi-
tional phases of meromeric duplication would
yield 24 segments (as in Scolopocryptopidae
in Scolopendromorpha) and the modal num-
bers of trunk segments observed in differ-
ent groups of Geophilomorpha. In geophilo-
morphs as a whole, numbers of segments are
separated into regular intervals of 2, 4, 8, or
16 segments (65). The model is largely con-
sistent with observed variation in trunk seg-
ment numbers across centipedes, although it
requires modifications to explain the common
pattern of 22 trunk segments found in most
scolopendromorphs.
Data on the identity of the Hox gene clus-
ter and Hox sequences in centipedes were
first generated for a scolopendromorph (38), a
lithobiomorph (15), and a geophilomorph (6).
Patterns of Hox gene expression are best doc-
umented in L. atkinsoni (46, 47). These stud-
ies show that centipedes have the complete
arthropod cluster of 10 Hox genes (47). Ex-
pression domains of myriapods are in some
respects intermediate between the broadly
overlapping domains of chelicerates and the
generally more restricted domains of insects
and crustaceans. The head-trunk tagmosis of
centipedes is marked by relatively restricted
expression domains in the head and maxilli-
pede and broad overlap of Ubx, Abd-A, and
Abd-B in the rest of the trunk, which corre-
sponds to its structural homonymy.
Expression patterns for other segmenta-
tion genes in L. atkinsoni generally show that
their roles are conserved across arthropods.
For example, even-skipped expression is similar
to that in other arthropods with short germ-
band embryos, showing strong posterior
expression stripes that fade anteriorly. The
initial study on expression of the segment po-
larity gene engrailed in a scolopendromorph
suggested that centipedes have unique pat-
terns compared with other arthropods (88).
Subsequent work on a lithobiomorph (45)
164 Edgecombe
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and a geophilomorph (14, 51a) instead shows
the typical arthropod expression of engrailed
stripes at the posterior end of segments. Ex-
pression of engrailed and other segmenta-
tion genes show that the centipede head is
composed of six segments (45), as is gener-
ally accepted for other mandibulate arthro-
pods. Sequence data derived from engrailed are
highly conserved between centipede orders,
although some instances of gene duplication
can be posited (5).
Conclusion
The segmentation process in centipedes has
mostly been studied to the stage when seg-
ment polarity genes are expressed (14, 51a).
Data are emerging on more upstream seg-
mentation genes, including homologs of the
Drosophila pair-rule genes (13, 45). Additional
work on these as well as other important
pattern-formation genes would help to clar-
ify the evolution of centipede segmentation.
SUMMARY POINTS
1. Morphology, molecular sequences, and combined analyses of both sources of data gen-
erally unite centipedes and other myriapods as a monophyletic group. In such schemes,
myriapods are sister to an insect-crustacean assemblage within the Mandibulata clade
(jawed arthropods).
2. Phylogeny based on morphology and sequence data from multiple molecular markers
shows that the addition of segments in postembryonic life history is a primitive trait for
centipedes. Similarly, the number of trunk segments in centipedes increased through
evolutionary time.
3. Fossil centipedes from the Paleozoic Era can be accommodated within living clades.
Along with their geological antiquity, certain centipede clades have ancient (e.g.,
Gondwanan) biogeographic distributions.
4. Recent studies of expression patterns of Hox and other genes show that centipedes
generally conform to segmentation mechanisms in other arthropods with short germ-
band embryos.
ACKNOWLEDGMENTS
We thank Doug Beckner for help in preparing the final figures. Fieldwork was funded by the
National Science Foundation under grant 0236871 and by Australian Biological Resources
Study grant 205–08.
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Contents ARI 24 October 2006 17:16
Annual Review of
Entomology
Volume 52, 2007
Contents
Frontispiece
Charles D. Michener ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp
xiv
The Professional Development of an Entomologist
Charles D. Michener ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp
1
Insect/Mammal Associations: Effects of Cuterebrid Bot Fly Parasites
on Their Hosts
Frank Slansky pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp 17
Phenology of Forest Caterpillars and Their Host Trees:
The Importance of Synchrony
Margriet van Asch and Marcel E. Visser ppppppppppppppppppppppppppppppppppppppppppppppppppp 37
Arthropod Pest Management in Organic Crops
Geoff Zehnder, Geoff M. Gurr, Stefan Kühne, Mark R. Wade, Steve D. Wratten,
and Eric Wyss pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp 57
The Sublethal Effects of Pesticides on Beneficial Arthropods
Nicolas Desneux, Axel Decourtye, and Jean-Marie Delpuech pppppppppppppppppppppppppppppp81
Impact of Extreme Temperatures on Parasitoids in a Climate Change
Perspective
Thierry Hance, Joan van Baaren, Philippe Vernon, and Guy Boivin pppppppppppppppppppp107
Changing Paradigms in Insect Social Evolution: Insights from
Halictine and Allodapine Bees
Michael P. Schwarz, Miriam H. Richards, and Bryan N. Danforth ppppppppppppppppppppp127
Evolutionary Biology of Centipedes (Myriapoda: Chilopoda)
Gregory D. Edgecombe and Gonzalo Giribet pppppppppppppppppppppppppppppppppppppppppppppp151
Gene Regulation by Chromatin Structure: Paradigms Established in
Drosophila melanogaster
Sandra R. Schulze and Lori L. Wallrath pppppppppppppppppppppppppppppppppppppppppppppppppp171
Keys and the Crisis in Taxonomy: Extinction or Reinvention?
David Evans Walter and Shaun Winterton ppppppppppppppppppppppppppppppppppppppppppppppp193
Yellow Fever: A Disease that Has Yet to be Conquered
Alan D.T. Barrett and Stephen Higgs ppppppppppppppppppppppppppppppppppppppppppppppppppppp209
vii
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Contents ARI 28 September 2006 19:28
Molecular Mechanisms of Metabolic Resistance to Synthetic and
Natural Xenobiotics
Xianchun Li, Mary A. Schuler, and May R. Berenbaum ppppppppppppppppppppppppppppppppp231
Group Decision Making in Nest-Site Selection Among Social Insects
P. Kirk Visscher pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp255
The Role of Allatostatins in Juvenile Hormone Synthesis in Insects and
Crustaceans
Barbara Stay and Stephen S. Tobe pppppppppppppppppppppppppppppppppppppppppppppppppppppppppp277
Nectar and Pollen Feeding by Insect Herbivores and Implications for
Multitrophic Interactions
Felix L. Wäckers, Jörg Romeis, and Paul van Rijn ppppppppppppppppppppppppppppppppppppppp301
Biology and Evolution of Adelgidae
Nathan P. Havill and Robert G. Foottit pppppppppppppppppppppppppppppppppppppppppppppppppppp325
Biology of the Bed Bugs (Cimicidae)
Klaus Reinhardt and Michael T. Siva-Jothy ppppppppppppppppppppppppppppppppppppppppppppppp351
The Use of Push-Pull Strategies in Integrated Pest Management
Samantha M. Cook, Zeyaur R. Khan, and John A. Pickett pppppppppppppppppppppppppppppp375
Current Status of the Myriapod Class Diplopoda (Millipedes):
Taxonomic Diversity and Phylogeny
Petra Sierwald and Jason E. Bond ppppppppppppppppppppppppppppppppppppppppppppppppppppppppp401
Biodiversity Informatics
Norman F. Johnson pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp421
Cockroach Allergen Biology and Mitigation in the Indoor Environment
J. Chad Gore and Coby Schal ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp439
Insect Conservation: A Synthetic Management Approach
Michael J. Samways ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp465
Interactions Between Mosquito Larvae and Species that Share the
Same Trophic Level
Leon Blaustein and Jonathan M. Chase pppppppppppppppppppppppppppppppppppppppppppppppppppp489
Indexes
Cumulative Index of Contributing Authors, Volumes 43–52 ppppppppppppppppppppppppppp509
Cumulative Index of Chapter Titles, Volumes 43–52 pppppppppppppppppppppppppppppppppppp514
Errata
An online log of corrections to Annual Review of Entomology chapters (if any, 1997 to
the present) may be found at http://ento.annualreviews.org/errata.shtml
viii Contents
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by HARVARD UNIVERSITY on 12/13/06. For personal use only.
