EVOLUTION & DEVELOPMENT 3:3, 170–205 (2001)
© BLACKWELL SCIENCE, INC. 170
Animal phylogeny and the ancestry of bilaterians: inferences from
morphology and 18S rDNA gene sequences
Kevin J. Peterson and Douglas J. Eernisse*
Department of Biological Sciences, Dartmouth College, Hanover NH 03755, USA; and *Department of Biological Science,
California State University, Fullerton CA 92834-6850, USA
*Author for correspondence (email: deernisse@fullerton.edu)
SUMMARY Insight into the origin and early evolution of the
animal phyla requires an understanding of how animal
groups are related to one another. Thus, we set out to explore
animal phylogeny by analyzing with maximum parsimony 138
morphological characters from 40 metazoan groups, and 304
18S rDNA sequences, both separately and together. Both
types of data agree that arthropods are not closely related to
annelids: the former group with nematodes and other molting
animals (Ecdysozoa), and the latter group with molluscs and
other taxa with spiral cleavage. Furthermore, neither brachi-
opods nor chaetognaths group with deuterostomes; brachiopods
are allied with the molluscs and annelids (Lophotrochozoa),
whereas chaetognaths are allied with the ecdysozoans. The
major discordance between the two types of data concerns
the rooting of the bilaterians, and the bilaterian sister-taxon.
Morphology suggests that the root is between deuterostomes
and protostomes, with ctenophores the bilaterian sister-
group, whereas 18S rDNA suggests that the root is within the
Lophotrochozoa with acoel flatworms and gnathostomulids
as basal bilaterians, and with cnidarians the bilaterian sister-
group. We suggest that this basal position of acoels and gna-
thostomulids is artifactal because for 1000 replicate phyloge-
netic analyses with one random sequence as outgroup, the
majority root with an acoel flatworm or gnathostomulid as the
basal ingroup lineage. When these problematic taxa are elim-
inated from the matrix, the combined analysis suggests that
the root lies between the deuterostomes and protostomes,
and Ctenophora is the bilaterian sister-group. We suggest that
because chaetognaths and lophophorates, taxa traditionally
allied with deuterostomes, occupy basal positions within their
respective protostomian clades, deuterostomy most likely
represents a suite of characters plesiomorphic for bilaterians.
INTRODUCTION
With the explosion of new developmental, paleontological,
and phylogenetic tools and data over the last 10 years, the
question of the origin and early evolution of animals has
never been more tractable, nor generated as much interest
from as many different fields of inquiry. However, a proper
understanding of animal evolution is predicated upon a
proper phylogenetic framework. As but one example taken
from a survey of Distal-less (Dll) expression among bilateri-
ans, Panganiban et al. (1997) argued that the latest common
ancestor of coelomate bilaterians utilized Dll in the develop-
ment of both its nervous system and in the developmental
pathway of some kind of “appendage.” This was inferred be-
cause all of the coelomate bilaterians analyzed (chordates,
echinoderms, onychophorans, arthropods, and annelids) ex-
pressed Dll in both places. Nematodes, however, lack a true
coelom and those studied to date lack appendages and ex-
press Dll only in the nervous system. Panganiban et al.
(1997) thus hypothesized that recruitment of Dll into ap-
pendage development is a coelomate apomorphy and expres-
sion in the nervous system a coelomate plesiomorphy, as-
suming that nematodes branched off the bilaterian line of
evolution before this latest common ancestor of coelomates.
If nematodes are, instead, members of a clade of molting an-
imals along with arthropods (Aguinaldo et al. 1997), the evo-
lutionary process hypothesized by Panganiban et al. (1997)
must be reexamined. Did the latest common ancestor of bi-
laterians (with or without a coelom) express Dll in both ner-
vous system and body wall outgrowths, and this was later
lost in the nematode lineage, or is the expression of Dll in
various bilaterian “appendages” convergent? Hence, a proper
understanding of animal evolutionary developmental biol-
ogy clearly requires knowledge of animal phylogeny (see also
Jenner 1999; Adoutte et al. 2000).
Many evolutionary scenarios (e.g., the trochaea theory of
Nielsen 1979, 1995) put forth to explain various aspects of
animal evolution rely on relationships derived from tradi-
tional morphological analyses. These analyses (e.g., Brusca
and Brusca 1990; Ax 1996; Nielsen et al. 1996; Schram
1997) usually find support for the following five hypotheses:
(1) annelids are closely related to arthropods; (2) brachio-