Table Of ContentUNRAVELING THE
HISTORY
Richard Brusca^
C,
ARTHROPOD
OF
BIODIVERSIFICATION^
Abstract
Current viovvs of arthropod phylogony are assessed in ligfit of recent research in morphological and molecular
phylogenetics, develo])men(al biology, neurobiology, and paleontology. Recent fossil discoveries and molecular clock
data inform us that arthropod diversification began in the Precanibrian, and suggest thai by the Cambrian the artFiropods
were already the most speciose inetazoan phylum on earth. The combination of metamerism and jointt^d appendages
(with intrinsic musculature), and the evolutionar) poteiUial of homeolic genes, has profoundly affected arthropod evolution
many
and created moq)tK)logical homoplasies. Kvidence strongly favors a monophyletic Arthropoda. Accumulating evidence
supp(»rts a hy[)othesis that insects and modern cnistaceans comprise a phylogenetic sister group, and that they, and jierliaps
Two
also Irilobites, chelicerates, and myria[K)ds, all ('(tuld have evolved out of an ancient crustacean stem line. im[>Iications
of this hypothesis are that Cmstacea coni[)rise a [)ara[)h)letic taxon and insects may be viewed as ''flying citislaceans."
Key words: Arthropoda, arthropod evolution, Cmstacea, insects, Metazoa.
PtU.KACE. The ChAELENGE of UNRAVEEI^G Emerging molecular studies have corroborated
Mt-:rA/()AN Phye()(;eny many, and challenged some, paradigms of metazoan
phylogeny. For example, whereas some molecular
made
Despite great progress in zoolog>' during
many studies have supported the long-held close rela-
the 20th century, there remain fundamental,
tionship between annelids and arthropods (Wheeler
unanswered questions concerning metazoan evolu-
The and al, 1993), recent studies have not done so (Lake,
tionary history. origins relationships of et
many animal phyla remain unclear or in dispute. 1990; Halanych et al., 1995; Eernisse, 1997; Agui-
In large part, this stems from the challenge of re- naldo et al., 1997). Furthermore, the discovery^ of
covering unambiguous phylogenetic signals from new animal phyla, and thus new fundamental body
ancient lineages. Recent molecular and paleonto- plans, continues to occur. The first edition of Lin-
among
logical studies suggest that major splits the naeus's (1735) Systema Naturae listed 14 groups
Metazoa occurred in the Precambrian, some per- that we now recognize as distinct animal phyla. To-
haps nearly a billion years ago (Wray et al., 1996; Jay, we recognize 34 animal phyla. Three former
Ayala et al., 1998; Seilacher et al., 1998; Li et al., phyla have recently been sunk: Pentastomids are
may
1998). In part, also be because the field of
it ^^^^ ^j^^^^j within the Arthropoda (allied with the
comparative morphology has popularity (and
lost
MaxiUopoda), and vestimentiferans and pogonoph-
And
employment emerg-
opportunities) the
finally,
^^^
^^^^^ ^^^ regarded as annelids (probably high-
new
i^ne field of molecular rphyloeDenetics is still so 11:1 u u inn-? &
/a* tj
/ i modined pol1 ychaet*es)\ (McHugh, 1997; iK>rusca jp
ly
. ,
improvements 1
that every year sees in the data an-
Brusca, in press).
alyzed and the phylogenetic inference methods
Most of the large-bodied animal groups were dis-
used. For example, prior 1997 most molecular
to
We
now
covered by the end of the 19th century. are
analyses were based on small numbers of taxa and
n on a track of discovery of microscopic metazoa, and
r r
r *u
shor_t^ sequences a si• ngl1 e gene, usually the i- n- ^ »
ot
^^'^^ "^^ ^^^™^^ ^^^" discovered just
rDNA P^y^^ ^^^.^
IBS
herently problematic gene. Recently,
l^^^: Gnathostomulida Loncifera
^^"^^
(1956),
however, new (and larger) molecular data sets have
and Cycliophora There a corre-
(1^83), (1995). is
been developed based on other conserved nuclear
new
lotion between the discovery of animal phyla
genes, mitochondrial gene order, and gene dupli-
and their body sizes: phyla described in the period
Because
cation data. unlikely that a single
is
it
1901-1920 maximum 3-
have body
gene will recover the full phylogeny of Metazoa, the of lengths of
mm; 1941-
future will no doubt see analyses of multiple gene 10 phyla described in the period of
maximum mm;
sets. 1960 have body lengths of just 1
I'his pap(M- benefited from reviews by Wendy Moore, Lisa Nagy, and an anonymous reviewer. Tfiis work was sup-
'
NSF-PEKT
ported in part by an grant (DP]B-9S2I649) to tbe autbor. S})e(ial thanks go to \\w indefatigable Peter Haven
for erieouraging the writing of this paper.
^ Columbia University, Bios[)here 2 Center, P.O. Box 689, Oraile, Arizona 85623, U.S.A.
Ann. Bor. Card. 13-25. 2000.
MissoL'Ki 87:
14 Annals the
of
Garden
Missouri Botanical
phyla described in the 1980s and 1990s have max- Tabic 1. Fossil record of major arthropod groups.
=^
imum mm.
body lengths of less than 0.5 Most of
Tardigrades: Middle Cambrian present
the small-bodied phyla are meiofaunal, although lo
^^"y^hophora: Middle Cambrian present
cycliophorans live as commensals on the mouth ap- to
& Early Cambrian Permian
to
pendages of various marine crustaceans (Funch
^''^f''^'
Xiphosura: Early Ordovician/Silurian present
to
The
Kristensen, 1997). discovery of these minute
Eurypterida: Ordovician through mid-Permian
F^arly
animals presents challenges to those of us interest-
Upper
Arachnida: Silurian to present
They
ed in animal phylogeny. are so small that a
Pycnogonida: Devonian present
to
great deal of their anatomy reduced or otherwise
is
Cambrian
Crustacea: Eariy Vendian)
(or to pres<^nt
We
know
altered. almost nothing about their de- Hexapoda: I^wer Devonian
present
to
velopmental biology, and they are so rare that mo- Myriapoda: Upper Silurian present
to
lecular biologists have not yet extracted gene se-
quences from them. predict that the discovery of
I
new
microscopic phyla continue another
will for
Recent work (Waggoner, 1996) suggests that even
half-century.
the Ediacaran (Vendian) fauna, of the Pre-
latest
The
challenges of unraveling animal phylogeny
cambrian, included early arthropod taxa, perhaps
are not unique to molecular biology, small animals,
true Crustacea.
new
or phyla. Biology has a long history of skir-
Ever since Darwin, biologists have asked the
mishing over phylogenetic issues at all levels. The
"How
question, has the incredibly successful
di-
evolutionary history of the Arthropoda has been one
Why
come
versification of arthropods about?" are
of the most challenging issues biologists struggled
many
there so arthropods? there something "spe-
Is
What
with throughout the 20th century. follows
is
What
cial" about these animals? the phyloge-
is
an update (as of mid 1998) on what we know about
Arthropoda?
netic history of the Specifically, are
arthropod evolutionary
history.
the arthropods monophyletic and what are the re-
lationships of the major arthropod groups one
to
Arthropod Background
Evolution:
another? There have been four great challenges
to
answering
biologists in these questions. Until
(1)
There are five clearly distinguished groups of ar-
the last decade of the 20th century, there had been
thropods: trilobites (extinct since the end of the Pa-
a lack of hypotheses on arthropod evolution based
~
4000
leozoic; described species); Chelicerifor-
on
principles of explicit phylogenetic inference.
(2)
mes
(horseshoe crabs, eurypterids, arachnids,
We
have a very incomplete understanding of
~ ar-
pycnogonids; 75,000 described
living species);
thropod development, though improving
this
is
crustaceans (crabs, shrimp, isopods, and their kin;
quickly with the advent of molecular developmental
~
50,000 described hexapods
living species);
(in-
biology. There has been a paucity of compre-
(3)
and 878,000
sects their kin; to 1.5 million de-
hensive studies based on fossils from the earliest
scribed and myriapods
living species); (centipedes,
ages of arthropod evolution Precambrian and
~ (late
millipedes, and 14,000 described
their kin;
liv-
early Paleozoic). apparent that high levels
(4) It is
And,
ing species). there are two close allies of the
homoplasy among
of exist the arthropods. In just
arthropods, tardigrades (water bears) and ony-
the past 10 years, major discoveries have begun
to
chophorans and The
{Peripatus their kin). close re-
address each
of these challenges, as discussed be-
lationship between the Tardigrada and the Arthrop-
low.
&
oda has never been seriously questioned (Brusca
Work
by the great comparative biologist Robert
Brusca, 1990), and recent molecular work contin-
Snodgrass in the 1930s established a benchmark
ues to support a sister-group relationship between
in arthropod biodiversity research. Table 2 shows a
now
these two phyla (Garey 1996). There are
et al.,
classification of the arthropods at that time, and
it
known
1.02 to 1.64 million described arthropods,
one most
this classification that finds in
is still
from virtually all environments on earth. Estimates
modern The
biology textbooks. Snodgrass
classifi-
of undescribed arthropod species range from 3
to
embraces
cation three important hypotheses:
100 The
million. arthropods (Table comprise
1)
85%
about of all described metazoan species. Arthropods comprise a monophyletic taxon
(1)
The
arthropods also encompass an unparalleled (2) Myriapods and hexapods form a sister group, a
range of structural and taxonomic diversity, have a taxon called Atelocerata (= Tracheata, or Uni-
rich fossil record, and have become favored ani- ramia of some authors). The Atelocerata have
mals of evolutionary developmental biology. Arthro- been united by several seemingly powerful
at-
among
pods were the animals
earliest to evolve. tributes:
Volume Number
Brusca 15
87,
1
2000
Arthropod
Biodiversification
1aM(^ 2. (Massifiralion of llir nrthn>[)ods and llioir allies sensu Snodgrass (19.*^f5)
Plnluni
Aiilir()[>()(la
Sul)|)li\luMi IVilohita
Snl>[»li}lunt Chclii^fiala
Class Mrrosluiiiala
Siilxlass Xiphosiita. llorseslioe crabs
Siihclass Klin plcrida. Kur\[)lrri(ls; rxllnci I'aleo/.oic arthropods
Land
Class Arachnida. spidrrs, miles,
etc.
Class Pyenogofiida. Sea sj)iders
Mandihnlata
Sniijtii}
UiFii
(]lass Criislacea. (^rahs, sliiiinps, isopods, etc.
Class Tracheata (= Atelocerata)
Subclass Ih'xapoda
Prolurans
Supcr(»itlcr Proliiia.
Superoidcr hisecta. Insects
Subclass Myria[)oda
Su[)erordcr (ienlipedes
Cbil()[»oda.
Superorder
Diplctpoda. Milliptnles
Superordcr lans
S\iiiplivla. Syrii[>li\
Pauropodans
SujxTor'der
l*aiir"o|K)da.
A
tracbcal system. clonal antibody raised against a specific glycopro-
rcs[)irat()i7
(a)
Uiiiratnous b'gs. tein (3G6), to crystalline cones, eucones, and other
(I))
Use of Malpighian tubules for excretion. elements in a variety of insect and crustacean ret-
(c)
—
&
Loss of the second head appt^ndagcs the inas (Edwards Meyer, 1990)
(d)
second antennae^ (as name Atelocerata im- was not until the late 1980s that Snodgrass's
tlie It
Vrslig*'s of the atdag(*n of this appendage long-standing view of arthropod relationships began
plies).
can be seen during the etnbt^ogeny of some to be seriously questioned with: the appearance
(1)
insects Sharov, 19S3; Bniktnoser, 1965). of explicit morphological and molecular phyloge-
(<'.g.,
amazing
rhc Crustacea and the Traclu'ala form a sister netic analyses, the discovery of the po-
(2)
(3)
—
name homeobox
Manihbidata Snod- genes arthropod develop-
group, a diat tential of in
tlie
couum ment and evolution, the emergence of
grass tnmsell
if (3)
lii 1.
molecular- based evolutionary developmental biol-
For a brief period of time in mid-century the
tlu*
C
ogy, and the discovery of exquisite new am-
(4)
championed
concept polyphyh'tic Aidiropo<la,
of a
brian preservations from Sweden, China, and else-
mainly by Manton and Anderson, enjoyed
S.
I).
wnhere.
&
some Manton
popularity (Manton, 1973, 1977;
and Anderson
Anilerson, 1979; yXnderson, 1979),
morphologicai. pnvlogenetic studies of
The Mantonian
(199G) maintains this view.
still
Ahthkopods
view of arthropods jdaced the myriapods, h<*xapods,
and (mych()j>horans in a separate lineage (Manton s Morphological phylogenetic studies of the arthro-
phylum "Uniramia") with an origin apart from the pods are summarized in Table 3. Overall, these
rest of the arthropods. However, this idea, based on analyses suggest three important ccmclusions:
flawed armnn(Mitation and an inade-
phylo*!;enetic
/ix *• .
rr-ihe art,tnopodis are a monophiylei tie taxon.
II (II
I
. r
. 1 1 •
quate embnoloiiical loundation, did not long sur-
^ /o\ tI-ihe reli at•ionsihi• p olr .tihe /C^rust. acea *to .tuhe m• sects
(2)
„
.,.
. . and, mod,ern
Vive the rigors scientinc testing
of
and myriapods ambiguous; Snod-
that
is is,
methods of phylogenetic inference (see below). In
Mandibulata a taxon of questionable
grass's
is
Perm-
adiUtion phylogt^netic analyses, studies
to
(»f
validity.
(Knkalova-Peck,
diaphatiopteroid insects
ian
+
The monophyly
of the Atelocerata (insects
(3)
& Bramkmann,
Kukalova-Peck
1991a, 1992;
1),
myriapods) also questionable.
is
1990) have shown that early pterygotes probably
num-
Waggoner
possessed polyramous appendages, further under- (1996) included in his analysis a
mining the Marilon-Anderson Uniramia hy{)odiesis. ber of arthropod-like fossils belonging to the "Ven-
Addilional support ailhropod monophyly has dian fauna," from the latest Precambrian (= Edi-
for
conie frotn studies of compound eyes using a mono- acara Period) that had generally been regarded as
16 Annals of the
Garden
Missouri Botanical
Table Morphological views of monopliyly within the arthropods.
3.
Artliropoils MaiKlibulates Tracheata
Year Author(s) nioiiophyhnic monophyh^tic monophylolic
&
1990 Brusca Brusca Yes Yes
n.a.
No
1991 iram Yes
Sci n.a.
19<)2 Eernisse Yes
et al. n.a. n.a.
993 Backeljau Yes
1 et al. n.a. n.a.
Wheeler Yes Yes Yes
et al.
994
Wills Yes Yes Yes
1 et al.
No No
1995 Ye
Wills
el al. s
Y Y
996
Nielsen Yes es es
1 et al.
1996 Waggoner Yes No No
&
1997 Emerson Schran Yes No No
1
No No
19<;8 St raus fehl Yes
He
"problematica." also included 21 Cambrian ar- taceans longitudinal connectives are pioneered by
modem He
thropods, and various taxa. concluded segmental neurons, whereas in the centipede Eth-
that: (a) the Arthropoda are monophyletic, (b) the mostigmiis ruhipres longitudinal connectives are pi-
Ediacaran arthropod-like fossils are, in fact, true oneered from neurons in the brain that send their
arthropods, and (c) the anomalocarids (and their axons posteriorly to set up the parallel connectives,
kin) fall out very close to the base, and are probably This difference between centipede and insect-
the most primitive known arthropods. Anomalocar- tacean ventral nervous systems compounded by
is
ids were giant predatory arthropods (arguably, true the fact that the pattern of segmental neurons in
Crustacea) that reached a meter in length. They are centipedes is quite different from that found in in-
known Cam-
from both the Precambrian and the sects and crustaceans; centipede ganglia receive
brian, and they were probably the largest predators contributions from more widely distributed
Chen
of that time (Briggs, 1994; et al., 1994). rons, and there are more neurons in the centipede
The most recent phylogenetic analysis of arthro- ventral cord when segmental axons are laid down.
pods was based on anatomical features of the cen- Comparisons of early neuronal outgrowth during
nervous system embryonic development and
tral (Strausfeld, 1998). Strausfeld of the brain thoracic
used 100 conserved neural charac;ters in the brains ganglia also suggest a close affinity between crus-
of a variety of segmented invertebrates to recon- taceans and insects (Harzsch et 1997; Theri-
al.,
among
struct phylogenetic relationships the arthro- anos 1995; Whitington 1991). Paulus
et al., et al.,
pods. His analysis suggested that insects and cms- (1979) argued for arthropod monophyly on the basis
taceans comprise a sister group, that the myriapods of shared characters in the organization of photo-
are a polyphyletic group (i.e., chilopods and dip- receptors and their satellite cells in compound and
He
lopods are not sister taxa), and that pycnogonids single-lens eyes. further noted that insect and
are true chelicerates. The most important neuronal crustacean ommatidia, with their developmentally
synapomorphies of Crustacea—Insecta are elements fixed numbers of cells, share more fine structural
and
of the optic lobes mid-brain, particularly fea- characters than either do with the chilopod om-
tures of the midline neuropils and neuropils asso- matidia (which comprise an indeterminate number
compound
ciated with the eyes. This analysis cor- of elements).
roborated earlier neurological descriptive work by
Strausfeld et al. (1995), which also concluded that Molecular
Pfiylogenetic Studies oe
insects are closer to crustaceans than to any other
AR'rin{<)lM)DS
arthropod group.
All arthropod central nervous systems use the Molecular phylogenetic studies of the Arthropo-
same fundamental embryonic plan of construction da are summarized in Table 4. Field et al. (1988)
Thomas rRNA
(Whitington et al., 1993; et al., 1984; sequenced a short segment of 18S but used
Strausfeld, 1998). However, a fundamental distinc- representatives of just 10 phyla (only 4 of which
between embryonic development were
tion the early of arthropods). Despite limitations, the Field
its
+
the myriapod nervous system and that of insects et al. work was pioneering. It was the first molec-
crustaceans was recognized some time ago. Whi- ular phylogenetic study to test the monophyly of the
tington el al. (1991) found that in insects and cms- arthropods, which supported, and the work ini-
it
Volume Number
Brusca 17
87,
1
2000
Arthropod
Biodiversification
Tal>le 4. Moh^-ular views of moiiophyly williin tlie arthropods.
+
Myriapoda
+
Hexapoda
Arthropods Crustacea
Year Hexapoda (Traeheata) Data
Aulli()r(s) iiiono[>hvlelic
rUNA
No
1988 Field et al. Yes Ye s 18S
7 No
1989 Yes \ es IHS rFiNA
Patti^rtion
rRNA
No No
1990 Lake Yes 18S
Y Y iRNA
No
1990 18S
Field es es
et al.
iRNA
No
1991 Turheville es Yes IHS
et al
rRNA
No
992 Ballard Yee>s Yes 12S
1 et al.
(milocliuntlrial)
rDNA
992 Winiiepenninckx Yes \ es IHS
n.a.
et al.
1
rDNA
1993 Van de Peer Yes Yes 9 IHS
et al.
•
rUNA +
1993 Yes Yes No IHS
\^lieeler nl)i(iuitin
et al.
rDNA
1995 ^'iniiepenninekx Yes Yes IHS
n.a.
et al.
& Ye No 18S + 28S rDNA
1995 Fried rieh laut/ Ye;S
Y Y rDNA
1996 Garev es n.a. 18S
ft al.
& Y Y No +
1997 Regier Shullz El -la rOI.II
v.^
rDNA
No 18S
19<)7 Eeriiisse es es
Ye.^
& rDNA
No
1997 Spears Allele Ye. Yes 18S
The
tiated a stream of follow-up studies, continuing to sister group to a paraphyletic Crustacea,
rRNA rDNA
18S sequences, and later the 18S Spears and Ahele analysis also strongly supported
gene Each subsequent study has tended malacostracan monophyly. Eernisse (1997) ana-
to
itself.
use more taxa and longer nucleotide sequences for lyzed 103 sequences and concluded that the
(1)
data base, but until very recently most also con- Arthropoda are monophyletic, but only if the tar-
its
18S
tinued to rely on the 18S gene. Problems associated digrades are included [probably another arti-
with the 18S gene, use of short gene sequences, fact], and hexapods are more closely related to
(2)
and single-gene phylogenetic inferences are well crustaceans than they are to myriapods, Regier and
known and need not be repeated here. Further- Shullz (1997) made a complete and welcome break
more, although there are now over 300 metazoan with the 18S gene, using sequences from two other
18S sequences available, most published phyloge- nuclear genes, the elongation factor (EF-la) gene
RNA
nies have been based on fewer than 20 sequences and the polymerase (POLII) gene. These
II
(Eernisse, 1997). This is despite studies that sug- trees were robust and mostly in agreement with the
minimum
gest a of 30-4-0 taxa are needed to ac- 18S work, concluding that: Arthropods are
(1)
curately identify the root node of a large clade (Le- monophyletic, Crustacea are paraphyletic, and
(2)
1993a, Sanderson, 1996; group myriapods,
cointre et al., b; Hillis, insects are not the sister of the
(3)
methodological and sampling
1996). In spite of but arose from within the Crustacea,
problems, recent molecular studies are beginning Recent work by Boore (1995) examined not
et al.
some However,
to converge on similar conclusions. gene sequences, but the linear arrangement of mi-
as Spears and Abele (1997) pointed out, ". in the tochondrial genes. This new type of data corrobo-
. .
among
crusade for understanding relationships rates the gene sequence work and recognizes a mi-
rDNA
crustacean and other arthropod lineages, the tochondrial gene arrangement that unique to the
is
and Holy
data represent but a not the Grail and
relic, crustaceans insects alone,
itself." In summary, the majority opinion from the mo-
The most recent 18S sequence data suggest that lecular research, and the most recent opinions from
myriapods
insects share fewer similarities with the both the morphological and molecular work, rec-
than they do with the Crustacea. Spears and Abele ognize four key features in arthropod phylogeny:
analyzed 31 18S sequences, and their re-
(1997)
suggested that neither crustaceans nor insects Arthropods are monophyletic.
sults (1)
When removed "prob- Neither the Mandibulata nor the Atelocerata
were monophyletic. they the
(2)
lematic" long-branched crustacean taxa (Remlpe- are natural groups
+
Cephalocarida, Mystacocarida), a myriapod Crustaceans and insects constitute a sister
dia, (3)
clade emerged with insects as the group, exclusive of the myriapods.
chelicerate
first,
18 Annals the
of
Garden
Missouri Botanical
Crustacea are likely to constitute a paraphyletic product of a single homeobox gene, the Ultrabi-
(4)
taxon. thorax (Uhx) gene (Carroll, 1995).
A
good example
of the evolutionary potential of
These
last three conclusions are in conflict with
homeobox
genes is seen in the abdominal limbs of
150 years of morphology-based thinking. Thus, two
insects. Abdominal limbs ("prolegs") occur on
lar-
new
profound implications of these studies that
vae of various insects in several orders, and they
the morphological attributes linking insects to niyr-
are ubiquitous in the order Lepidoptera, cat-
i.e.,
lapods might be convergences uniramous
all (e.g.,
erpillars. Abdominal limbs were almost certainly
legs, tracheal system, Malpighian tubules), and that
Hence
present in adult insect ancestors. prolegs
insects are actually "flying crustaceans" the
(in
may
have reappeareil in such groups as the Lepi-
same
sense that birds are flying reptiles).
doptera through something as simple as the de-re-
pression of an ancestral limb drveh)pment program
Emerging Views from Developmentai.
Studies
We
they represent an now know
(i.e., atavism). that
The
unique combination of segmentation and proleg formation Is initiated by a <4iang(' in the reg-
jointed appendages has allowed arthropods to de- ulation and expression of the BX-C gene complex
modes
velop of locomotion and feeding, and body the Bithorax complex, which includes the Hox
(i.e.,
region specialization, unavailable to other metazoan genes Ubx, abdA, and ahdB) during embryogenesis
We
now know
phyla. that the fates of these seg- (Carroll, 1995).
mental units and their appendages are under the Molecular and developmental biology also seem
ultimate orchestration of homeotic genes. These to have broken the deadlock on the arguments over
genes select the critical developmental pathways to origins of uniramous and biramous limbs Po-
(e.g.,
be followed by cells during morphogenesis. Ho- padic et al., 1996; Panganiban et al., 1995, 1997;
meobox &
genes determine such basic body architec- Shubin al, 1997; Emerson Schram, We
et 1997).
ture as the dorso-ventral and the anterior-posterior now know that limb branching a second-order
is
body where body appendages and phenomenon,
fonn, the probably orchestrated largely by the
i
,
&
general types of appendages that form (Averof homeobox gene Distal-less This single gene
(Oil).
Patel, 1997; Panganiban et al., 1997; Shubin et al., initiates development of unbranched limbs in in-
Homeobox
1997). genes can either suppress limb sects and branched limbs in crustaceans. Antibod-
development, modify
or it to create alternative ap- ies that recognize Dll proteins sh(jw t^xprcssion at
A
pendage
morphologies. growing body of evidence the tips of insect limbs and also in biramous crus-
suggests that these unique genes have probably tacean limbs (Panganiban Branched
el al., 1995).
played major roles in the evolution of new body limbs are formed wwnhen me gene expressed ec-
tl is
1
among
plans arthropods and the Metazoa in general topically in Drosophiln (Diaz-Benjumea
et al.,
&
(Davidson et al., 1995; Williams Nagy, 1995; 1994). In fact, Dll occurs in many animal phyla.
Panganiban
et 1995). where expressed body
al., is at tlu* tips of ec'todfTmal
it
The degree to which homeobox genes have been outgrowths in such different structures as the limbs
conserved is remarkable, and most of them proba- of vertebrates, parapodia and anleimae of poly-
bly date back at least to the Cambrian. For exam- chaete worms, tube feet of echinoderms, siphfms of
pie, homologues of the Pax-6 gene seem to dictate tunicates, and appendages of arthropods. Further-
where
eyes will develop in all animal phyla. Pax- more, recent work suggests that whether an arthro-
6 is so similar in protostomes (insects) and deu- pod mandible "whole-limb" many
is (i.e., built of
terostomes (mammals) that the genes can be ex- segments) or "gnathobasic" built of only the
(i.e.,
perimentally interchanged and
function basalmost
still segnuuits) also dep<*nds on the expres-
Homeobox
correcdy. genes modulate the expression sion of the gene Distal-less. Thus, Dll expressed
is
of dozens of interacting, downstream, developmen- in the whole limb (or multisegmented) jaws of myr-
tal genes whose products drive morphogenesis. The iapods, but not in the griathobasic jaws of crusta-
—
profound homeobox
evolutionary potential of genes and
insects further testimony the
still to
lies in this hierarchical nature. Variation in the out- probable sister-group relationship of insects and
put of these multigene networks can many
Crustacea.
at
k_T V->
simply by
levels, tinkering with the relative timing
—
of gene expression an evolutionary process we
Paleontoi OGK DATA
TllE
Al
know
as heterochrony. To understand profound
the
homeobox
potential of genes to drive evolutionary Recent work has shown the fossil record of ar-
change, consider that within the Drosophila genome thropods dates back to the early Cambrian, or per-
85-170
different genes might be regulated by the haps the late Precambrian. Ancl, by the mid-Paleo-
Volume Number
Brusca 19
87,
1
2000
Arthropod
Biodiversification
Table Some important Prerambrian and Cambrian arthropod Lagerstatten faunas.
5.
Name
Age
Principal location
Orsten fauna Upper Cambrian (-510 MYA) Southern Sweden
MYA)
Burgess Shale fauna Middle Cambrian (--520 British Columbia
Chengjiang fauna Lower Cambrian (—530 MYA) Soutllern Chin a
(-560-600 MYA)
Ediacaran fauna Latest Precambrian Ediacara Hills, Aust.
known members many
zoic, all five arthropod lineages were in existence tons, including the first of
modem
and had already undergone substantial radiation. groups. However, the arthropods that
is
it
Arthropods are also the land animals for which dominate this fauna, including trilobites and bra-
first
we have a geological record (Labandeira et doriid "crustaceans" (and also tardigrades and on-
al.,
1988; Kukalova-Peck, 1990), and by the Late Si- ychophorans). The largest of the Chengjiang ani-
known
and myriapods mals Anomalocaris, from Ediacaran
scorpions also
lurian the first terrestrial is
already present. In fact, both terrestrial and and Middle Cambrian deposits (Briggs, 1994). The
marine myriapods have been reported from this pe- Chengjiang fauna very similar to that of the Bur-
is
(Almond, 1985; Hahn 1986; Labandeira gess Shale, and demonstrates that the arthropods
riod et
al., it
1988), although molecular data suggest that were already far advanced by this early date.
et al.,
myriapods might have arisen as early as the Cam- The spectacular recent discovery by Klaus Miill-
&
brian (Friedrich Tautz, 1995). The centipede er and Dieter Walossek (MuUer, 1983, 1992; Muller
first
&
fossils occur in the Upper Silurian {- 414 MYA) Walossek, 1985; Muller et al., 1995; Walossek
&
and, along with trigonotarbid arachnids, constitute Muller, 1992, 1997) of microscopic arthropods
known land animals (Jeram from the Upper Cambrian Orsten deposits of Swe-
the earliest et
al.,
1990). The millipede fossils occur in Devonian den, has brought to light a rich fauna of minute
first
and cms-
deposits (Almond, 1985; Robison, 1990); they are crustaceans, crustacean larvae, various
Among
similar to the extant genus Craterstigmus (Shear et tacean-like arthropods. them, fi)r example,
1984) and are contemporaneous with the Skara, a cephalocarid-, or mystacocarid-like
first is
al.,
terrestrial mites, pseudoscorpions, and scorpions crustacean for which both naupliar lanae and
(St0rmer, 1969, 1977; Shear et 1987), as well adults have been recovered (the nauplius larvae are
al.,
as the hexapods (Greenslade, 1988). The ear- only a couple hundred microns long; adults are
first
mm &
liest known fossil hexapods are bristletails and col- about 1 in length) (Muller Walossek, 1986).
lembolans from 390-million-year-old Gaspe mud- Sham, and many other Orsten Crustacea, were sure-
modem
stone (Labandeira et al., 1988). Some good records ly meiofaunal animals not unlike marine
now
of these early creatures exist, and the presence meiofaunal crustaceans.
of these predatory arthropods suggests that complex Fossils from this Cambrian site in Sweden have
who
terrestrial ecosystems were in place at least as early been collected since the days of Linnaeus, ac-
as the late Silurian. Perhaps the most important tually described the first fossils from this area in
ancient arthropod fossils are those in which even 1757 (trilobites and conodonts). However, a brand-
—
MuUer
new began and Wal-
the soft parts of the animal were p d the kind of collecting with
new
so-called ancient Lagerstatten (Table ossek s work in the 1980s. This Orsten material
5).
The
These ancient fossils have pushed the age of or- is all microscopic, three-dimensional fossils.
igin for the arthropods back to at least 600 MYA, Orsten arthropods show little or no signs of decom-
and they provide us with critically important data position. They presence details less than 1 micro-
on early arthropod anatomy and evolution. These meter in size (e.g., cuticular pores, the bristles on
extraordinary faunas are now telling us that Cms- setae). Dozens of Orsten microcmstacea have so far
tacea probably predate the appearance of trilobites been described. The recovery of these three-dimen-
in the fossil record, mnning counter to a long-held sionally preserved animals and the developmental
belief that trilobites were the most ancient arthro- series that have been found (with successive larv^al,
—
pods. The recently exploited Chengjiang fauna of juvenile, and adult instars in animals less than 1
mm
south China Lower Cambrian, about 10 million in length) have provided us with infomiation
is
years older than the Middle Cambrian Burgess on the detailed anatomy of body segments and ap-
many The
Shale fauna (Chen 1994). The Chengjiang pendages of ancient stem-arthropods. Or-
et al.,
Cambrian Cmstacea had
fauna very well preserved and includes at least sten fauna shows that all
is
modem
100 species of animals, many without hard skele- the attributes of cmstaceans, such as com-
20 Annals of the
Garden
Missouri Botanical
pound eyes, a head shield, naupliar larvae (with localities that have yielded pentastomids, and thus
now
locomotory antennae), and biramous append- the conodonts (also long a mystery, but widely
first
ages on the second and third head somites (the sec- regarded as parts of early fish-like vertebrates)
ond antennae and mandibles). might have been the original hosts of the pentasto-
Taken work
together, this recent paleontological mids.
corroborates Whitington's observations long ago
Cam-
about the Burgess Shale fauna, that during Tmk Onycmophora
brian limes the non-trilobite arthropods were both
As
with pentastomids, onychophorans, were
too,
morphologically more varied and more numerous
amazing, early-Cambrian, explosive ma-
We P^^ ^^ ^^^
than w(^re the trilobites (despite popular belief).
They have been found Bur-
^^"^ diversification. in
now know
also that arthropods have pn.bably been
Cam-
Shale-type faunas at several locdities, in
the dominant animals in terms of species diversity S^^^
'*"^" deposits from China and Siberia, and in the
since the Cambrian. Arthropods comprise over one-
&
Swedish Orsten fauna (Xianguang Weiguo, 1988;
third of species described from Lower Cambrian
all
& &
Xianguang Junyuan, 1989; Ramskold Hou,
strata.
l^^)- ^^ ^"^^ Conway
^"^^' "^^^ Morris's
Briggs and Fortey ^^^'^^
(1989) cladistically analyztnl
'anginal reconstruction of Hallucigenia (from the
23 Cambrian
of the arthropod taxa, plus 5 extant
Burgess Shale) had the animal turned upside-down,
groups. Tlieir tree placed the Crustacea at the veiy
Ramskold Hou
and
(1991) recently turned Hallu-
base, as a paraphyletic sequence of taxa, and
""'S^^rua over and found a second pair of legs, con-
placed and
the trilobites chelicerates near the top
clmling was an onychophoran with long dorsal
of the The most recent molecular work does it
tree.
^"^ onychophoran known
^"
^^^^^^^ '^«^'
not conflict with this tree, in viewing the Crustacea ^^P^"^^^' '^
Chcngjiang China
^^^"^ ^he deposits of with side
as a paraphyletic group from which the other major
&
and (Ramskold Hou,
plates spines 1991). Ay-
arthropod clades emerged.
sheaia (also from the Burgess Shale) was originally
described Waleott as an annelid, but too,
l)y is
it,
Pkntastomida
TiiL
now
regarded an marine onychophoran.
as early
Pentastomids
are obligatory parasites of verte-
CONCLUSIONS
brate respiratoiy systems. There are about 100 de-
scribed which
species, all of infest various tetra-
now
Let us return our two fundamental ques-
to
pods, including two cosmopolitan species
that
Why
regarding arthropod
tions evolution: are there
humans. The
blood-sucking
infest adults inhabit re-
many
so arthropods, and what the phylogenetic
is
spirator}^ tracts of their hosts, where they anchor
As
history of the arthropods? the question,
to
first
themselves by means of their hooklike head ap-
propose over-arching scenarios, each complex
six
I
pendages. For years was b<*lieved that pentasto-
it
own
in its right.
mids were onychophorans
allied with the as ver-
miform, pre-arthropod However, The
creatures. several (1) ical superiority of arthropods not
is
recent molecular studies (using 18S gene sequenc- a recent event. Recent fossil discoveries, and
es) have revealed the pentastomids to be highly molecular clock data, inform us that arthroood
modifiinl crustaceans (Abele 1989, 1992; began
et al., diversification very early in the histor)'
Garey
et al., 1996). Corroborative independent of the Metazoa, in the Precambrian, and by the
work over the past few years has come from cla- Cambrian the arthropods were probably already
distic analyses of sperm and lar\'al morphology. the most speciose metazoan phylum on earth.
nervous system anatomy, and cuticular fine strui:- Arthropods have been on a powerful phyloge-
ture (Wingstrand, 1972, 1978; Storch, 1984; Storch 600 MY. They
netic trajectory for well over
&
Jamieson, 1992). Furthemiore, Miiller and Wal- have had a great deal of time to radiate, and
ossek s work on the Swtnlish Orsten fauna proves with the exception of the trilobites and the eu-
that tlu* pentastomids (and also the tardigrades) had rypterids, the major lineages have survived
all
aj^jpeared at least by the Upper Cambrian, long be- and continue
radiate.
to
fore die land vertebrates had even evolved (Muller (2) Their great size range, especially on the smaller
& &
Walossek, 1988; Walossek Muller, 1994). So, end of the scale, adapts arthropods for a great
we
must ask what the original hosts of these para- The Cambrian
variety of ecological niches. Or-
sitic crustaceans might have been. Walossek, Miill- sten deposits tell us that a whole fauna of in-
and even Stt^phen Jay Gould have noted
er, that terstitial/meiofaunal arthr(»pods already existed
common
Conodont Cambrian
fossils are in all the as early as the mid-Cambrian, and this habitat
Volume Number
Brusca
87, 21
1
2000
Arthropod
Biodiversification
has continued to he rich in adaptive radiation that Crustacea are a paraphyletic group, and that
and speciaHzed species ever since. Similar Crustacea and Insecta are very closely related
tlie
small-hody-size niches are filled in a great to one another, hut not to the Myriapoda. In fact,
We
many
specialized environments today. find the insects appear have arisen from within a
to
high diversities of minute arthropods in hahitats crustacean stem line. Further, recent molecular and
among
such as marine sediments, coral reefs, fossil data are beginning to suggest that the trilo-
the fronds of algae, on mosses and oth(^r prim- bites, chelicerates, insects, myriajjods, and recent
itive plants, and on the bodies every kind of cnistaceans all might have emergtM] from crusta-
f)f
animal imaginable. There are even arthropod cean stem-line ancestors. This view of a paraphy-
faunas that live strictly on the gills of other letic Crustacea spinning off a series of otlier major
crustaceans (mites and small crustaceans). arthropod lineages might explain why morpholo-
Small insects and mites have exploited virtually gists have been unable to come to agreement on the
every terrestrial microhabitat availabh^ sister-group relationships of the major ailliropod
The close relationship and coevolution with lineages. Resolution of this conflict will come,
(3) I
flowtTing (on land) and algae aquatic predict, within the next two decades, with further
j)lants (in
environments) have been a powerful force urnlerstanding of the genetic regulation of devel-
in
new
the radiation of the arthropods. not just the oj)mental processes, examination of nuclear
It is
insects that have been on a coevolutionar)' tra- and mitochondrial genes (and use of multiple gene
—
many and more
jectoiy with plants crustaceans utilize data sets in phylogenetic analyses), as
algae as both a living substrate and a food cladistic analyses include fossil species, particu-
source and show strong evidence of coevolu- larly the growing series of Chengjiang, Or.sten, and
related arthropods.
tion.
The arthropods (insects) were the flying an-
first
(4)
them
imals, and the ability to fly led into niches \
SPtx:L I.ATION
other inveitebrates simply could not penetrate.
Metamerism (the serially repeated body seg- The realization that insects might have arisen out
(5)
many
ments and appendages of arthropods) provides of an ancestral crustacean stem line leads to
new
an enormous amount of easily manipulated implications concerning arthropod evolution.
body plan material upon which evolutionary For example, given this scenario, on(* could search
among
processes can Given the great ag(% sheer about the Crustacea for a likely ancestor to
act.
diversity, and our emerging knowledge of reg- the insects and in doing so recognize the presence
"
ulatoiy genes in tht^se animals, a high level of of a 4"4.fixed" 19-segmented body plan in insects and
homoplasy no longer certain crustaceans (or more likely a 20-segmenttMl
surjirising.
is
The potential for major changes in body plans plan in each, Kukalova-Peck, 1991a, b; Scholtz et
(6)
due homcobox and 1994; Scholtz, 1995). All insects arc fixed on
variations genes, the al.,
to in
downstream genes they regulate, just begin- this body plan. Of all the crustacean higher taxa,
is
body plan consistently occurs (mly the sub-
ning to be realized, but this potential is clearly this in
Eumalacostraca^the
enormous. There seems doubt chang- class crabs, shrimps, isopods,
that
little
and their kin. Thus, the insects did evolve from
es in homeotic genes over time have profoundly if
a crustacean ancestor, one might speculate that
affected arthropod evolution. C(msidering the
they could have evolved from a eumalacostracan.
number and position of limbs in arthropods,
homcobox Examining the Eumalacostraca for a possibh^ insect
and and
the flexibility of regulatory
switches, wonder that arthropod an- ancestry, there is only one group that is truly ter-
is litth^
it
has evolved gas-exchange tracheae
(grant-
restrial,
atomical diversity s(H^ms so endless.
ed, probably convergently to those of insects), has
—
As to the scc(md question what is the phylo- reduced/lost one pair of ant(^nnae (antennae one re-
—
genetic histoiy of the Arthropods seems the duced in oniscideans, antennae two reduced in
it
homcobox
plasticity of the arthropod body and gene hexapods), and has strictly uniramous walking legs
—
may
expression have produced an even higher level (as do the insects) the tenestrial isopods (Isopo-
of homoplasy than <mce thought. As a result, some da: Oniscidea). Could be that insects are not only
it
traditional morphological classifications are in con- flying crustaceans, but flying isopods?
with molecular classifications. All the evidence The concept of a Eumalacostraca-Insecta sister-
flict
com-
suggests that the arthropods are monophyletic. group relationship finds strong support in
th<^
However, fossil data, recent comparative neuroan- paratlve anatomy of arthropod central nervous sys-
compound
atomical research, and molecular data all suggest terns. Developm(^nt of the eye follows
Annals
22 the
of
Garden
Missouri Botanical
similar morphogenetic events in insects and eu- a close malacostracan-insect relationship, includ-
&
malacostracans (Hafner Tokarski, in press). In ing differences in tagmata arrangement and loca-
addition, the optic lobes of pterygote insects and tions of the gonopores. The fossil record also does
+
eumalacostracans are distinguished by nested reti- not support an isopod insect sister-group rela-
The known
notopic neuropils, each of which represents the tionship. oldest isopod fossils are only
whole eye. In these two taxa, these neuropils com- 300 million years in age (Phreatoicidea: Hesslerella,
&
prise an anatomically distinct lamina, medulla, and Carboniferous) (Brusca Wilson, 1991). However,
lobula complex (Strausfeld, 1996). The presence of a recent analysis of phreatoicidean phytogeny sug-
these structures in pterygote insects and eumala- gests the isopods might have had their origin con-
&
costracans was viewed as a homology indicating a siderably earlier than this (Wilson Keable, in
sister-group relationship between these taxa by press), and further examination of this unconven-
may
Osorio and Bacon (1994) and Nilsson and Osorio tional idea be warranted.
(1997). Further, eumalacostracans that have so far
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its
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