Blackwell Publishing LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Linnean Society of London, 2006? 2006
148?
585602
Original Article
HYBRIDIZATION IN EVOLUTIOND. I. WILLIAMSON
Zoological Journal of the Linnean Society, 2006, 148, 585–602. With 11 figures
Hybridization in the evolution of animal form and
life-cycle
DONALD I. WILLIAMSON*
14 Pairk Beg, Port Erin, Isle of Man IM9 6NH, UK
Received June 2005; accepted for publication December 2005
Examples of animal development that pose problems for Darwinian evolution by ‘descent with modification’ but are
consistent with ‘larval transfer’ are discussed. Larval transfer claims that genes that prescribe larval forms originated in adults in other taxa, and have been transferred by hybridization. I now suggest that not only larvae but also
components of animals have been transferred by hybridization. The ontogeny of some Cambrian metazoans without
true larvae is discussed. The probable sequence of acquisition of larvae by hemichordates and echinoderms is presented. I contend (1) that there were no true larvae until after the establishment of classes in the respective phyla,
(2) that early animals hybridized to produce chimeras of parts of dissimilar species, (3) that the Cambrian explosion
resulted from many such hybridizations, and (4) that modern animal phyla and classes were produced by such early
hybridizations, rather than by the gradual accumulation of specific differences. © 2006 The Linnean Society of
London, Zoological Journal of the Linnean Society, 2006, 148, 585–602.
ADDITIONAL KEYWORDS: Cambrian explosion – component transfer – echinoderms – larval transfer –
trilobites.
INTRODUCTION
Hybridogenesis, the generation of new life-forms by
hybridization, includes both larval transfer (Williamson, 2001, 2003) and component transfer. In the
present paper, I propose that component transfer preceded larval transfer in animal evolution, and that it
was largely responsible for the ‘Cambrian explosion’.
This term refers to the first appearance of a very wide
assortment of animal fossils in upper Vendian and
lower Cambrian strata, including the first known
examples of most modern phyla and representatives of
other taxa that became extinct. The Vendian–Cambrian boundary is now placed at 543 Mya, and the
principal events of evolutionary interest were probably 550–530 Mya (Conway Morris, 2000).
Darwin (1859) admitted that the sudden appearance of many types of animals in ‘the lowest known
fossiliferous strata’ posed grave difficulties for his theory of gradual evolution by ‘descent with modification
through natural selection’. He suggested, however,
that the apparent outburst in animal form was largely
illusory, and it probably resulted from imperfections in
*E-mail: [email protected]
the fossil record. He considered it ‘indisputable that
before the lowest Silurian stratum was deposited, long
periods elapsed, as long as, or probably far longer
than, the whole interval from the Silurian age to the
present day; and that during these vast periods the
world swarmed with living creatures’. (Darwin substituted ‘Cambrian’ for ‘Silurian’ in the last edition of The
Origin of Species.) This view receives some support
from Bromham et al. (1998), who concluded that
‘[molecular] data are not compatible with the Cambrian explosion hypothesis as an explanation for the
origin of metazoan phyla, and provide additional support for an extended period of Precambrian metazoan
diversification’. Many others, however, agree with
Conway Morris (2000) that ‘the Cambrian explosion is
real and its consequences set in motion a sea-change
in evolutionary history’.
Conway Morris continued, ‘Although the pattern of
evolution is clearer, the underlying processes still
remain surprisingly elusive’. I accept that the Cambrian explosion is real, and I suggest that the principal underlying cause was hybridization between many
diverse types of early animals, before any species had
acquired larvae. The molecular evidence does not necessarily conflict with this view.
© 2006 The Linnean Society of London, Zoological Journal of the Linnean Society, 2006, 148, 585–602
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D. I. WILLIAMSON
LARVAE, METAMORPHOSIS, AND LARVAL
TRANSFER
Embryos are unhatched forms of animals or plants.
Larvae are immature postembryonic forms of many
animals that develop into different forms by metamorphosis. Darwin (1859) said that ‘larvae are active
embryos’, but I claim that larvae came first in phylogeny, and embryos are inactive larvae. Metamorphosis
is a marked change in form during ontogeny. A
juvenile animal grows into an adult without
metamorphosis.
Animals in different taxa employ many diverse
methods of metamorphosis, but first I wish to distinguish between ‘metamorphosis by substitution’, in
which one body-form is replaced by another, and
‘metamorphosis by addition’, in which the first bodyform becomes part of the second. The vast majority of
modern animals with larvae metamorphose by substitution, and no larval characters survive the process.
As illustrated below, Cambrian animals with so-called
larvae metamorphosed by the addition of a new bodyform to the hatched form.
Most modern biologists have followed Darwin (1859)
in assuming that adults and their larvae evolved from
the same genetic stock by ‘descent with modification’.
Darwin presented no evidence for this view, here
referred to as the ‘same stock’ theory, but virtually all
phylogenetic trees of the animal kingdom published
since the early 20th century are based on this assumption. Many confirmed observations, however, are
incompatible with the ‘same stock’ theory, but they are
consistent with the larval transfer theory, which infers
that larvae were later additions to life-histories.
Balfour (1880–81) believed that most larvae are
‘secondary’, i.e. they ‘have become introduced into the
ontogeny of species’, but he was unclear on the sources
of larvae. My larval transfer hypothesis, in its original
form, stated that genes prescribing the basic forms of
some larvae had been transferred from other taxa by
hybridization (Williamson, 1988, 1992). In its present
form it proposes that genes prescribing the basic forms
of all larvae and embryos originated as adults in other
taxa and that they were transferred by hybridization
(Williamson, 2001, 2002, 2003). This implies that larvae were acquired only after the major adult taxa were
established, and, in the present paper, I consider the
effects of hybridization before the major taxa were
established. Hybridogenesis and symbiogenesis, the
generation of new organisms by symbiosis (Margulis,
1993), both involve fusion of lineages, whereas Darwinian ‘descent with modification’ is entirely within
separate lineages. Natural selection works on the
results of all forms of evolution.
The main evidence for larval transfer may be
divided into four categories: (1) multiple larvae, (2)
incongruous larvae, (3) recently evolved larvae, and
(4) metamorphosis. Some examples from each category are briefly discussed here, and are described
more fully, together with many more examples, in
Williamson (2003).
MULTIPLE
LARVAE
Many animals go through two or more larval phases in
their development. A molluscan trochophore, for
example, always metamorphoses into a shelled veliger
which, in turn, metamorphoses into a juvenile mollusc, a barnacle nauplius metamorphoses into a cypris
larva which metamorphoses into a juvenile barnacle,
and a crab zoea usually metamorphoses into a megalopa which metamorphoses into a juvenile crab. Some
insects, including oil-beetles (Meloidae), go through
three distinct larval phases before pupating into the
form from which the adult emerges. Penaeid, sergestid, and euphausiid shrimps go through four larval
phases before becoming juveniles.
Darwin (1859) was aware that barnacles pass
through two larval phases and penaeid shrimps pass
through four before becoming juveniles, but neither he
nor anyone else has suggested how these life-histories
might have evolved by ‘descent with modification
through natural selection’. Most sergestids and
euphausiids are planktonic throughout life, so there is
no obvious advantage in having a planktonic larval
phase, let alone four. Strathmann & Eernisse (1994)
did not consider larval transfer, but they interpreted
DNA evidence as suggesting that nauplius larvae
were later additions to the life-histories of penaeid,
sergestid, and euphausiid shrimps. I claim that all larvae were later additions to life-histories and that multiple larvae resulted from several hybridizations in
the same adult lineage. It is proposed, for example,
that the four larval phases of penaeid shrimps (nauplius, protozoea, mysis, and postlarva) were acquired by
ancestral penaeids that hybridized with an adult naupliomorph, an adult plenocaridean, an adult mysidacean, and an adult penaeid-like animal, not
necessarily in that order. The taxa Naupliomorpha
and Plenocaridea were proposed by Williamson
(2001), the former for nauplius-like adults (see below
under ‘Cambrian “Larvae”’) and the latter for animals
resembling the Cambrian genus Plenocaris Whittington, 1974 (Briggs, 1983).
INCONGRUOUS
LARVAE
If larvae and corresponding adults had evolved from
the same genetic stock, larval and adult classifications
should be compatible, but many larvae are incongruous in that they seem to belong to a different taxon
from the adult. A crustacean example concerns the
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HYBRIDIZATION IN EVOLUTION
sponge-crab Dromia (Dromiidae). Its zoea larva
closely resembles that of the hermit-crab Pagurus
(Paguridae), but adult Dromia and Pagurus are classified in different infraorders. This is explicable if an
ancestor of Dromia had acquired zoea larvae by
hybridizing with an ancestor of Pagurus.
The hydrozoan genus Hebella (Fig. 1) provides a
striking example from the phylum Cnidaria. The lifehistories of many hydrozoans include a sessile hydroid
phase and a planktonic medusoid phase, and the
hydroids and medusoids of the same species are usually regarded as having evolved from a common ancestor, like larvae and adults. Most marine larvae are
planktonic, but in the Hydrozoa the planktonic phase
(the medusa) is also the phase that reproduces sexually. In the present context it is immaterial whether
the hydroid or the medusa is considered to be the
larva. Hydroids of the order Thecata have hydrothecae
into which the polyps can retract; they typically have
leptomedusae, which are saucer-shaped and develop
gonads on their radial canals. The order Athecata consists of hydroids without hydrothecae; they have anthomedusae, which are bell-shaped and develop gonads
on the manubrium (mouth tube). Hydroids of the six
species of Hebella are classified in the order Thecata,
suborder Lafoeida (Fig. 1A), but only H. parasitica
587
and H. furax are known to have a medusoid phase.
The medusa of H. parasitica (Fig. 1B) is an anthomedusan, characteristic of the order Athecata, which is a
different order from the hydroid from which it came.
The medusa of H. furax (Fig. 1C) is a leptomedusan,
characteristic of the order Thecata, but it is classified
in the suborder Campanulinida, a different suborder
from its hydroid. The two medusae are in different
orders. This makes a mockery of conventional classification, and it seems inexplicable on the assumption
that hydroids and their corresponding medusae
evolved from the same genetic stock. It is, however,
consistent with the theory that hydroids and medusae
were originally distinct taxa, and hybridizations
between members of these taxa produced animals
with hydroid and medusoid phases in the same lifehistory. In the case of H. parasitica and·H. furax, the
hydroids must have acquired their medusae from very
different sources.
RECENTLY
EVOLVED LARVAE
In the example just cited, it seems inescapable that
either H. parasitica or·H. furax or (more probably)
both hydroids acquired their medusae after the genus
Hebella had divided into its constituent species. Other
A
B
C
Figure 1. Hydroid and medusae of Hebella (Hydrozoa: Thecata). A, gonophores of H. parasitica; B, male and female medusae of H. parasitica; C, medusa of H. furax. (A, B adapted from Boero, 1980; C adapted from Migotto & de Andrade, 2000.)
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D. I. WILLIAMSON
examples of congeneric adults with very different larvae are known in the Echinodermata and the Crustacea. Such recent acquisitions are incompatible with
the evolution of larvae and adults from the same
stock, but they show that some larvae at least were
later additions to life-histories.
METAMORPHOSIS
Under the larval transfer hypothesis, metamorphosis
by substitution represents a change from one taxon to
another during development, the taxa being those of
the two animals that hybridized to produce one animal
with two developmental phases. The discardment of
all larval organs at metamorphosis is difficult to reconcile with the theory that larvae and adults diverged
gradually from the same stock and each step was subject to natural selection. The metamorphosis of echinoderms and bryozoans are examples chosen from
many diverse kinds of metamorphosis by substitution,
not only because they illustrate contrasting methods
of transformation but also because they are relevant
to later sections of this paper. I shall present molecular evidence consistent with the theory that echinoderm larvae were not acquired until after the
respective classes of echinoderms were established,
and I shall suggest that no larvae were acquired in
any phylum until after the classes of the respective
phyla were established. The life-history of bryozoans
gives an indication that component transfer was an
essential factor in the evolution of this phylum, and I
shall propose that component transfer was an essential factor in the evolution of all phyla.
In echinoderms, the radially symmetrical juvenile
develops from undifferentiated cells (stem cells) lining
one or more of the coelomic sacs of the bilaterally symmetrical larva. The juvenile eventually migrates to the
outside of the larva, and at this stage it is able to move
quite independently of the swimming movements of
the larva. In most cases the larva then settles and
degenerates, and it is usually absorbed by the growing
juvenile. In some starfish, however, the juvenile drops
off the swimming larva, and in Luidia sarsi (Fig. 2A)
the larva may continue swimming for a further three
months (Tattersall & Sheppard, 1934). During this
time the same individual, from the same egg, exists in
two remarkably different forms, the bilateral swimming larva and the radial crawling juvenile. Other
examples of overlap between larva and juvenile of the
same individual occur (1) in polychaete worms with
trochophore larvae (Fig. 2B), in which the wriggling
segmented worm protrudes from the swimming larva,
(2) in nemertean worms with pilidium larvae
(Fig. 2C), and (3) in doliolid salps with tadpole larvae
(Fig. 2D). In each case the juvenile and larva move
independently, and the juvenile may break free while
the larva continues swimming. The coexistent juveniles and larvae clearly have separate nervous systems, and, in doliolids, they have separate brains. I
know of no proffered explanation of how one animal,
with one genome, might have evolved into two coexistent forms which are clearly neither twins nor
clones. Such occurrences, however, are consistent with
the suggestion that the basic forms of larvae were
acquired by hybridization, and therefore two genomes
are involved. The two coexistent body-forms represent
those of the two animals that hybridized. I believe that
the first echinoderm larvae were acquired when an
adult echinoderm hybridized with an adult acornworm (enteropneust hemichordate), an ancestor of
which had acquired larvae by hybridizing with an
adult planctosphere (see below under ‘The sequence of
larval transfers’). The first trochophore and pilidium
larvae were acquired when animals in at least seven
phyla hybridized with adult rotifers resembling Trochosphaera, or with animals that had earlier acquired
larvae by hybridizing with such rotifers. The first
doliolid tadpole larvae were acquired when a doliolid
hybridized with an adult appendicularian. Cases in
which the larva and juvenile overlap are interpreted
as showing that the two genomes involved may be
expressed simultaneously during part of the ontogeny
of the respective animals.
Experimental cross-fertilizations of ascidian eggs
with sea-urchin sperm (Williamson, 2003) and of seaurchin eggs with ascidian sperm (Williamson, in
press) have provided further evidence of the independence of larval and adult forms. Pluteus larvae, resembling those of the respective sea-urchin parents,
developed in both cases. In the first experiment, a
minority of the plutei from ascidian eggs grew into fertile sea-urchins, while the majority retracted their
arms to became spheroids of about 0.2 mm which did
not develop further. In the second experiment, all the
plutei from sea-urchin eggs became spheroids of diameter 0.1–0.2 mm. A few of these came to resemble juvenile ascidians but did not develop further. Many of the
spheroids in the second experiment divided repeatedly, and some grew into irregular shapes of up to
6 mm.
The ‘start again’ metamorphosis of some animals
contrasts with the foregoing examples of overlapping
metamorphosis. Some bryozoans of the class Gymnolaemata have unshelled trochophore larvae (Fig. 3A)
and some have shelled cyphonautes larvae (Fig. 3B).
The occurrence of two very different types of gymnolaemate larvae poses problems for the ‘same stock’
theory, but the method of metamorphosis from both
types of larvae is the same. The larva settles and then
undergoes histolysis and cytolysis until no larval
organs or tissues remain. The larval cells form two
connected capsules, and they all revert to the stem cell
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HYBRIDIZATION IN EVOLUTION
589
B
A
C
D
Figure 2. Examples of overlapping metamorphosis. A, Luidia sarsi (Echinodermata): swimming bipinnaria larva and
detached juvenile starfish; B, Polygordius sp. (Annelida): two stages showing segmented polychaete worm protruding from
swimming trochophore larva; C, Cerebratulus sp. (Nemertea): juvenile nemertean worm within swimming pilidium larva;
D, Doliolum mulleri (Urochordata): juvenile doliolid tunicate within cuticle of tadpole larva. Juvenile stippled in each case.
(A, C adapted from Williamson, 1992; B, D adapted from Borradaile et al., 1935.)
stage. The juvenile grows from these dedifferentiated
cells: the main body from one capsule, and the lophophore from the other (Fig. 3C). Lophophores are prominent feeding organs, and each consists of ciliated
tentacles enclosing the mouth. They also occur in several other animal phyla. The separate development of
the bryozoan lophophore from the rest of the animal
may have important evolutionary implications (see
below under ‘Component transfer’).
The ‘start again’ method of metamorphosis is
another phenomenon that has never been adequately
explained in terms of the Darwinian ‘same stock’ theory. Under this theory, adult and larval bryozoans
must have diverged gradually from a postulated
ancestral form to such an extent that no larval organs
or tissues could be modified into adult organs and tissues, and we are asked to believe that this method of
development, including the drastic metamorphosis,
evolved ‘by means of natural selection’. Under the lar-
val transfer theory, bryozoan adults and larvae did not
evolve from the same stock. The first bryozoan trochophore larva resulted from hybridization between a
bryozoan and a Trochosphaera-like rotifer. The first
cyphonautes larva resulted from hybridization
between a bryozoan and a cyphonautes-like animal
which has no modern counterpart. This animal probably resembled an inarticulate brachiopod without a
lophophore. Such animals are, as yet, unknown, but if
lophophores can be transferred (see below under
‘Component transfer’) they might well have existed.
The drastic ‘start again’ method of metamorphosis in
bryozoans suggests that the animals that provided the
larval forms were widely different from bryozoans.
COMPONENT TRANSFER
Lophophores, as mentioned earlier, occur in several
taxa: the four phyla Bryozoa, Phoronida, Brachiopoda,
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D. I. WILLIAMSON
A
B
C
Figure 3. Bryozoan larvae and adult. A, trochophore larva of Alcyonidium; B, cyphonautes larva of Membranipora;
C, adult zooid of Electra. (After Williamson, 1992.)
and Entoprocta, and the class Pterobranchia of the
phylum Hemichordata. A lophophore is a sophisticated organ, and it seems unlikely to have evolved
more than once, but not all groups with lophophores
seem to be closely related. This is fully discussed by
Willmer (1990), and is reflected in the general lack of
agreement on the composition of the taxon Lophophorata. The Entoprocta, previously regarded as a class of
bryozoans, are today usually excluded not only from
the Bryozoa but also from the Lophophorata because
the anus opens within the lophophore. It opens outside
in all other lophophorates. The Pterobranchia are usually included with the Enteropneusta in the phylum
Hemichordata (Fig. 4), but while pterobranchs have
lophophores, enteropneusts do not. Fortey, Briggs &
Wills (1996) refer to a Chinese upper Vendian species
which bears a remarkable resemblance to the ptero-
branch Rhabdopleura, while the first record of a
phoronid is ‘doubtfully Pennsylvanian’ (upper Carboniferous), some 300 Myr later. The phoronids are widely
regarded as being close to the basal stock of the lophophorates, but they were the last to appear in the fossil
record. The difficulties in trying to explain the inheritance of lophophores in terms of Darwinian evolution
and the curious method of development of the lophophore in bryozoans (from a different capsule from the
main body) led me to suggest that this organ may have
been transferred between taxa by hybridization (Williamson, in press). More evidence would probably be
gained by crossing an animal with a lophophore and
one without.
The suggestion that lophophores have been transferred between taxa raises the possibility that
other parts and organs of animals have also been
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HYBRIDIZATION IN EVOLUTION
A
C
591
B
D
E
F
G
H
Figure 4. Enteropneust and pterobranch hemichordates and a planctosphere. A–E, enteropneusta: A, adult Dolichoglossus, B, tornaria larva; C–E, stages in metamorphosis; F, G, Pterobranchia: F, adult Rhabdopleara; G, pterobranch larva. H,
Planctosphaeromorpha: adult Planctoshaera pelagica. Scale bar = ∼10 mm (A), ∼1 mm (B–E, G), ∼5 mm (F, H). (Adapted
from Borradaile et al., 1935; Hyman, 1959.)
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D. I. WILLIAMSON
transferred. While there is evidence that some larvae
have been acquired from other taxa comparatively
recently (see above under ‘Recently evolved larvae’),
this is not the case for components of adult animals.
There have probably been sporadic hybridizations
between organisms ever since the evolution of sex. I
suggest that early animals had spare genome capacity,
and hybridizations between them produced animals
with components from two or more sources. The
resulting hybrids and their descendants were concurrent chimeras, and those that metamorphosed did so
by addition (see below under ‘Cambrian larvae’). Later
animals had little spare genome capacity, and hybridizations between them led to the transfer of bodyforms which appeared sequentially in the life-history
of the hybrid and its descendants, one form as the
larva, the other as the adult. Such animals with larvae
are sequential chimeras (Williamson, 1991), and they
metamorphose by substitution.
A
CAMBRIAN ‘LARVAE’
Nauplii occur as a larval phase in many crustaceans.
They have one pair of uniramous preoral appendages,
two pairs of similar biramous postoral appendages,
and usually a small median eye (Fig. 5A). Crustaceans
other than nauplii have two pairs of preoral antennae,
a pair of postoral mandibles which do not resemble
antennae, a variable number of postmandibular
appendages, and usually a pair of compound eyes.
Metanauplii have the same functional appendages as
nauplii and, in addition, have rudimentary appendages that will become functional in the next developmental phase; these rudiments do not resemble the
functional appendages.
There are no known Palaeozoic metanauplii. Several species of fossil nauplii were described from upper
Cambrian strata in southern Sweden by Müller &
Walossek (1986a). These included 67 specimens of one
B
C
Figure 5. A, nauplius of Penaeus sp. (recent Crustacea: Penaeidae). B, C, Martinssonia elongata (upper Cambrian): B,
paranauplius II (left first appendage omitted); C, oldest known stage. Scale bar = ∼0.1 mm (A after Gurney, 1942; B, C
adapted from Müller & Walossek, 1986b.)
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HYBRIDIZATION IN EVOLUTION
species, ‘larva A’, from 16 different samples in three
different stratigraphic zones, covering some 30 Myr.
In spite of the range in place and time, the specimens
are remarkably similar and show no growth variation.
This is consistent with the view that ‘larva A’ was not
a larva but an adult (Williamson & Rice, 1996). The
absence of Cambrian metanauplii and the differences
between the appendages of nauplii and crustaceans
(sensu stricto) led me to propose that Cambrian
nauplii were not larvae but members of the Naupliomorpha, a taxon of noncrustacean arthropods
(Williamson, 2001). My suggestion that various crustaceans later acquired nauplius larvae by hybridizing
with naupliomorphs explains the lack of correlation
between the occurrence of nauplius larvae and the
classification of crustacean taxa (Williamson, 2003).
Martinssonia elongata Müller & Walossek (1986b)
was a noncrustacean arthropod from the upper Cambrian of Sweden (Fig. 5B, C). Each of the three smallest described stages resembled a nauplius (Fig. 5A) in
having one pair of uniramous appendages followed by
paired biramous appendages, but while a nauplius has
two pairs of biramous appendages, the comparable
form in Martinssonia had a third pair (Fig. 5B). This
stage was termed a metanauplius by Müller &
Walossek (1986b), but, as the posterior pair of appendages were functional and resembled the other
biramous appendages, it does not conform to the usual
definition of a metanauplius. The term paranauplius
was substituted by Williamson & Rice (1996) and is
used here. Müller & Walossek described two later
stages thought to have developed from paranauplii,
the larger of which is shown in Figure 5C. It is
assumed that, after the last paranauplius stage, the
body elongated considerably and developed eight
somites and a terminal telson. Further biramous
appendages, similar to those of the paranauplius,
developed on the anterior somites. The position of the
first articulation between somites corresponds to the
posterior end of the paranauplius. The paranaupliar
appendages were retained, and the paranauplius
became the prosoma of the segmented animal.
The development of Martinssonia from a paranauplius was probably comparable to that from a nauplius
in the extant branchiopod crustacean Leptestheria
(Fig. 6) (Gurney, 1942; as Estheria), except that the
trunk appendages of Leptestheria do not resemble the
biramous naupliar appendages. In this genus the pair
of uniramous preoral appendages are very small at
hatching, and they disappear at the second moult. In
Leptestheria and other branchiopods, metamorphosis
to the adult form is gradual, and the postoral naupliar
appendages are retained. The branchiopod nauplius
becomes the prosoma of the segmented animal. This
contrasts with the development of other modern crustaceans with nauplii, in which metamorphosis is
593
sudden and no naupliar features are retained. I regard
adult branchiopods and Martinssonia as concurrent
chimeras, in which the genic recipe for a segmented
body was added to that for a nauplius/paranauplius by
hybridization. In both cases, metamorphosis is/was
gradual and by addition. Other modern crustaceans
with nauplii (apart from branchiopods) are sequential
chimeras, and they metamorphose by substitution.
Trilobites were Palaeozoic segmented marine
arthropods in which longitudinal grooves separated
the raised middle body from the lateral portions. The
appendages were jointed, and they consisted of a pair
of uniramous preoral antennae and a variable number
of similar biramous postoral appendages. The ontogeny of a number of species has been described (e.g.
Whittington, 1959). Development from the earliest
stage, the unsegmented protaspis, was by the gradual
addition of segments behind the protaspis, and many
protaspid features were retained (Fig. 7A–D). The protaspis became the prosoma of the segmented trilobite,
and metamorphosis was by the addition of body segments to the protaspis. I suggest that the first protaspides were adult animals, of which the naraoiid
pictured by Fortey et al. (1996) was an example. This
lower Cambrian species, from the Chengjiang fauna of
China, lacked free thoracic segments, and it resembled an enormously inflated protaspis. Fortey et al.
(1996) regarded such forms as adults, and suggested
that they had evolved from trilobites by paedomorphosis, maturing in the protaspid phase. I agree that they
were adults, but I submit that they were members of a
distinct taxon, the Protaspidomorpha, which evolved
before the trilobites. Protaspidomorphs lived in the
vicinity of segmented arthropod-like animals, and trilobites were created when representatives of these
types of animals hybridized to produce concurrent
chimeras. The Protaspidomorpha and the Naupliomorpha are in the same category as the Rotifera,
the Appendicularia (phylum Urochordata), and the
Planctosphaeromorpha (usually placed in the phylum
Hemichordata), which some authors have regarded as
persistent larvae but are better explained as distinct
phyla from which larvae were acquired by hybrid
transfer (Williamson, 2003).
The trilobite protaspis is often referred to as a larva,
but, like the paranauplius of Martinssonia and the
nauplius of Leptestheria, it becomes the prosoma of
the adult. In the vast majority of modern animals with
larvae, all larval characters are lost at metamorphosis
and the larva does not become a prosoma. I question
whether the name ‘larva’ should be applied to the initial free-living form which becomes a prosoma, and I
propose the name ‘protomorph’ for this pseudolarva.
Protomorphs become prosomas, but not all prosomas
develop from protomorphs. For example, an adult
enteropneust hemichordate, such as Dolichoglossus
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D. I. WILLIAMSON
Figure 6. Stages in the development of the branchiopod crustacean Leptestheria syriaca, to different magnifications.
(From Gurney, 1942; as Estheria.)
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HYBRIDIZATION IN EVOLUTION
A
B
D
595
C
E
Figure 7. Two Cambrian trilobites. A–D, stages in the development of Sao hirsute: A, protaspis; B–D, early segmented
stages. E, adult Agnostus pisiformis. Scale bar = ∼1 mm (A–D from Borradaile et al., 1935; E redrawn after Fortey, 2000.)
(Fig. 4A), consists of a prosoma (proboscis), mesosoma
(collar) and metasoma (trunk), but it hatches as a
blastula which develops into a tornaria larva (Fig. 4B)
which metamorphoses into the tripartite juvenile
worm (Fig. 4C–E). Adult pterobranch hemichordates
(Fig. 7F) are also tripartite, consisting of a prosoma
(proboscis), a mesosoma (lophophore), and a metasoma (trunk), but they develop from a larva resembling a trochophore (Fig. 4G) (Hyman, 1959)
Naraoia compacta, from the Burgess Shale of Canada, and Agnostus pisiformis (Fig. 7E), from European
Cambrian strata, are examples of trilobites in which
a second protaspis appears to have been added
posteriorly.
THE SEQUENCE OF LARVAL TRANSFERS
We can deduce more about the sequence of acquisition
of larvae in echinoderms than in other phyla, but
many deductions from echinoderms probably also
apply to other phyla. While it is rarely possible to put
geological dates on the acquisition of echinoderm larvae, it is possible to infer the probable sequence of
events. I agree with Balfour (1880–81) that echinoderms did not acquire larvae until after the classes of
the phylum were established, and I now propose that
animals in all phyla did not acquire larvae until after
the classes of the respective phyla were established.
Larvae of an acorn-worm (enteropneust hemichordate) and of the five classes of echinoderms with larvae are shown in Figure 8, and the sequence in which
I believe hemichordates and echinoderms acquired
larvae is summarized in Figure 9. I hold that the first
echinoderm larva was a doliolaria (Fig. 8B), acquired
by a sea-lily (Crinomorpha). The source of this barrelshaped larva is not known, but I suggest that it was a
barrel-shaped adult in an extinct deuterostome taxon.
Hybridization between this animal and a sea-lily produced a sea-lily with doliolaria larvae (Fig. 9). I claim
that tornaria larvae of acorn-worms (Enteropneusta)
and all echinoderm larvae other than doliolarias had
their origin in the Planctosphaeromorpha, of which
the only extant representative is Planctosphaera
pelagica (Fig. 4H). This species is often regarded as a
giant tornaria larva, supposedly capable of metamorphosing into an acorn-worm (as in Fig. 4B–E), but
none of the known specimens, including one of 25 mm,
showed any sign of metamorphosis. I maintain that it
is an adult in a distinct taxon, the Planctosphaeromorpha (Williamson, 2001), and that a former adult
planctosphere hybridized with an acorn-worm (phylum Hemichordata, class Enteropneusta) to produce
an acorn-worm with tornaria larvae (Fig. 8B). A seacucumber (phylum Echinodermata, class Holothuromorpha) then hybridized with a descendant of this
acorn-worm to acquire auricularia larvae (Fig. 8C).
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D. I. WILLIAMSON
B
A
D
E
C
F
Figure 8. Larvae of an enteropneust hemichordate and echinoderms. A, tornaria larva of an acorn-worm (Enteropneusta);
B, auricularia larva of a sea-cucumber (Holothuromorpha); C, bipinnaria larva of a starfish (Asteromorpha); D, echinopluteus larva of a sea-urchin (Echinomorpha); E, ophiopluteus larva of a brittle-star (Ophiuromorpha); F, doliolaria larva of a
sea-lily (Crinomorpha). Scale bar = ∼1 mm (Adapted from Williamson, 1992, 2003.)
Subsequently a starfish (class Asteromorpha) hybridized with a sea-cucumber to acquire bipinnaria larvae
(Fig. 8D), a sea-urchin (class Echinomorpha) hybridized with a starfish to acquire echinopluteus larvae
(Fig. 8E), and a brittle-star (class Ophiuromorpha)
hybridized with a sea-urchin to acquire ophiopluteus
larvae (Fig. 8F).
Pterobranch hemichordate larvae (Fig. 4G) resemble nonfeeding trochophores, and they must have had
a different origin from the larvae of enteropneusts.
The similarity of enteropneust larvae to echinoderm
larvae and affinities between the larvae of sea-cucumbers and starfish and between the larvae of seaurchins and brittle-stars have been recognized since
the 19th century. The larval link between enteropneusts and echinoderms led Haeckel (1866) to propose
that radial echinoderms were descended from bilateral hemichordate-like ancestors – an apparent example of his ‘biogenetic law’ that ‘ontogeny recapitulates
phylogeny’. Haeckel, however, was unaware that larvae of pterobranch hemichordates are quite unlike
echinoderm larvae, and he ignored the larval affinities
of the respective classes of echinoderms, which are
quite different from those of the adults. If larval affinities imply adult relationships, sea-cucumbers and
starfish should have evolved from one branch of echinoderms because they have similar auricularia-like
larvae, and brittle-stars and sea-urchins should have
evolved from another branch because they have similar pluteus larvae. Such suppositions, however, have
been dismissed by most echinoderm specialists, and
fossil evidence points to one branch of echinoderms
that gave rise to starfish and brittle-stars and another
that produced sea-urchins and sea-cucumbers (Smith,
1988). Balfour (1880–81) and Fell (1948, 1963, 1968)
both maintained that the larval affinities of enteropneusts and the classes of echinoderms do not reflect
adult affinities. Balfour rejected Haeckel’s theory on
the evolution of echinoderms from bilateral ancestors,
and he proposed that echinoderm larvae were
acquired after the respective classes were established.
Figure 9 takes into account the views of Balfour and
Fell and the fossil evidence. It also indicates hybridizations between early echinoderm-like animals to
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HYBRIDIZATION IN EVOLUTION
597
Figure 9. Reticulate phylogeny of adults and larvae of extant hemichordates and echinoderms, showing probable sequence
of events. Time (horizontal) not to scale. Ord/Sil, Ordovician/Silurian boundary; pres, present; thick black lines, adults; thin
black lines, larvae; grey arrows, larval transfers.
produce the echinoderm classes (see below under ‘Vendian and Cambrian animals’). The many extinct echinoderm classes (Paul, 1979) are not shown.
Fell (1948) described the direct development of a
New Zealand brittle-star in which the blastopore
becomes the mouth (i.e. it is a protostome). Several
other brittle-stars probably develop in a similar way,
and Fell (1963, 1968) proposed that this represents
the original method of echinoderm development. A
comparable case of direct protostomatic development
was described for a subAntarctic heart-urchin (Spatangoidea) by Schatt & Féral (1996). Figure 9 incorpo-
rates Fell’s view that echinoderms are protostomes,
the majority of which have acquired deuterostome larvae. It does not show hybridizations within classes,
leading to the spread of larvae, or cases in which there
were no hybridizations and the species concerned continued to develop directly as protostomes. It also fails
to show the minority of starfish, sea-urchins, and brittle-stars that have doliolaria larvae, but it gives some
indication of how this situation might have evolved.
Doliolarias are usually the only larvae in sea-lilies,
and they are the second larvae of sea-cucumbers,
appearing after the auricularia. Doliolarias never
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D. I. WILLIAMSON
occur in starfish with bipinnaria larvae or in seaurchins and brittle-stars with pluteus larvae, but they
occur as the only larva in a few species with abbreviated larval development in each of these classes. Most
starfish, sea-urchins, and brittle-stars probably have
genic recipes for both doliolarias and trochophorederived larvae, directly or indirectly acquired from a
sea-cucumber. Apart from sea-cucumbers, however,
these two larval forms are never both expressed in the
same life-history.
Syvanen’s phylogram (Williamson, 2002; Fig. 10),
based on 18S ribosomal RNA of adult animals and one
insect larva, appears to show the phylogeny of
enteropneust and echinoderm larvae rather than
adults. A review of the phylogenetic implications of the
18S gene by Abouheif, Zardoya & Meyer (1998) concluded that ‘the 18S rRNA molecule is an unsuitable
candidate for reconstructing the evolutionary history
of all metazoan phyla’, and this is borne out by Syvanen’s phylogram. It contains several unnatural
groupings, including that between an arrow-worm and
Figure 10. A phylogram of some metazoans, based on 18S
rRNA. (From Williamson, 2002; after Michael Syvanen,
unpubl. data)
a tick and another between an insect larva and a
bivalve mollusc. The evidence is consistent with the
view that the 18S ribosomal gene has been transferred
between taxa several times. That part of the phylogram that relates to enteropneusts and echinoderms
shows the same sequence as that deduced from larvae
(see above and Fig. 9), except that Syvanen did not
investigate pterobranchs, Plactosphaera or brittlestars. I submit that genes prescribing enteropneust
and echinoderm larvae were transferred together with
ribosomal genes in a series of hybridizations. The modern echinoderm classes were established by the end of
the Ordovician (Paul, 1979), so, if Balfour (1880–81)
and I are correct, echinoderm larvae were added in
later periods. An extension of Syvanen’s phylogram
(Fig. 10) to cover a pterobranch, Planctosphaera, and a
brittle-star with pluteus larvae would be of great
interest, and of even more interest if it also included a
direct developing brittle-star or heart-urchin that
develops as a protostome. A comparison of phylograms
based on different genes would also be welcomed.
I have already mentioned that the lack of correlation between the occurrence of nauplius larvae and
the classification of Crustacea is consistent with the
suggestion that nauplii were acquired after the main
crustacean taxa had evolved. The occurrence of
trochophore-like larvae in the Mollusca, Annelida,
Echiura, Sipuncula, Bryozoa, Nemertea, and Platyhelminthes presents a comparable case. The Echiura and
Sipuncula are not divided into classes, but the other
phyla are. Trochophore-like larvae occur in only some
members of three of the eight classes of Mollusca, and
in some members of only one class of each of the other
six phyla. Many biologists apply Darwin’s (1859)
maxim ‘community in embryonic [and larval] structure reveals community of descent’ to all phyla in
which trochophore and similar larvae occur. They contend that such phyla evolved from a common ancestor
with trochophore larvae, and that this larval form has
been ‘lost’ in most modern members. I, however, claim
that trochophores, like all larvae, were later additions
to life-histories, and their occurrence is consonant
with the view that they were added after the establishment of the classes of the respective phyla. Tornaria-like larvae occur in one of the two classes of
Hemichordata and four of the six classes of Echinodermata (see above), and I now propose that there were
no larvae in any phylum until after the establishment
of classes within the major phyla. I further submit
that there were Cambrian protomorphs but no larvae,
and that Cambrian hybridizations produced concurrent chimeras, of which Martinssonia and trilobites
are examples. More examples are discussed in ‘Vendian and Cambrian animals’ (below).
The complete genomes of several animals are now
known. The greatest number of protein-encoding
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HYBRIDIZATION IN EVOLUTION
sequences is 26 588, found in man, but animals in a
variety of phyla have more than half this number.
This seems to imply that there is a limit to the size
of genomes, but it would have taken some time to
reach this limit. I suggest that early animals had
spare genome capacity, and, as a result, late Vendian and early Cambrian hybridizations produced
concurrent chimeras, including the first members of
new phyla. This view of the sudden origin of phyla
contrasts with Darwin’s assumption that higher taxa
differentiated gradually by the accumulation of specific differences. Concurrent chimeras continued to
be produced in the later Cambrian and the Ordovician and probably in later periods, but smaller
ullage in genome capacity now led to new classes
rather than new phyla. Sequential chimeras (animals with larvae) appeared in subsequent geological
periods.
Another factor that probably facilitated hybridizations between early animals was their poorly
developed specificity. I assume that mechanisms to
encourage homosperm fertilization and to discourage
heterosperm fertilization would have been built up
gradually, and would have been rudimentary in early
animals.
VENDIAN AND CAMBRIAN ANIMALS
I believe that the first animals with tissues (metazoans) resulted from hybridizations between colonial
protistans and that there were several such forms
(Williamson, 2003). This is not at variance with the
views of Darwin (1859: 454), who ‘believe[d] that animals have descended from at most only four or five
progenitors’. These early animals were all marine and,
like the great majority of modern marine animals,
shed their gametes into the water, where fertilization
took place. I assume that heterosperm fertilizations
were relatively common, not only between the first
animals but also between the resulting hybrids. This
produced many concurrent chimeras, which included
the first members of most animal phyla, living and
extinct. Hybridization between animals at all levels of
diversity was the biological basis of the so-called Cambrian explosion (which started in the late Vendian). Of
course animal survival and diversification also
required suitable environmental conditions in some
parts of the world ocean, but a favourable environment does not explain the explosion of phyla. The
great expansion in numbers and diversity of animals
following the Triassic/Jurassic minimum produced no
new phyla or classes. Of those Vendian and Cambrian
heterosperm fertilizations that hatched, natural selection ensured that only some survived for long periods.
Many of those that became extinct during the Palaeozoic era survived long enough to have representatives
599
preserved in the Chengjiang deposits of China (lower
Cambrian), the Burgess Shale of British Columbia
(mid-Cambrian), and the ‘Orsten’ limestone of Sweden
(upper Cambrian).
I do not question that animal species have evolved
and are evolving gradually by Darwinian ‘descent with
modification’, within separate lines of descent. I do
question, however, whether animal phyla and classes
evolved in this way. I postulate that phyla originated
in the Cambrian explosion and resulted from hybridizations between disparate early animals. These phyla
were concurrent chimeras, or in the words of Valentine
(2004), ‘phyla have split personalities’. Classes, which
require less spare genome capacity than phyla, also
resulted from hybridizations between early animals,
and they continued to be produced in the late Cambrian and the Ordovician and probably later, after the
phyla were established. Modern phyla and classes are
those that survived natural selection. On this view,
animal phyla and classes are concurrent chimeras,
and I claim that the morphology of early animals is
consistent with this view.
The Burgess Shale fossils Laggania and Anomalocaris (Fig. 11A, B) were regarded as members of a
hitherto unknown phylum by Whittington & Briggs
(1982). Collins (1996) proposed a new arthropod class,
the Dinocarida, to accommodate them and some
related Chinese Cambrian forms, but whether they
fall within the Arthropoda depends on how this major
taxon is defined. The circular mouth with ‘teeth’
within the aperture resembles that of a chordate
cyclostome rather than an arthropod. Willmer (1990),
after a full discussion, concludes that the term ‘arthropod’ is ‘to be taken only as representative of a grade of
organization’, and ‘most available evidence suggests
that the three major phyla of modern arthropod-type
animals – Crustacea, Chelicerata, and Uniramia –
cannot be successfully united as a natural group’. This
is consistent with my view that all phyla and classes
had hybrid origins. The only described dinocarids are
large, so it is not known whether they hatched as protomorphs to which segments were added (as in Martinssonia and trilobites) or as segmented animals (as
in modern amphipod crustaceans). In either case, I
suggest that they were descended from hybrids
between dissimilar animals and that they were concurrent chimeras.
Many Cambrian animals combined characters of
two or more modern phyla, as exemplified by
Amiskwia and Nectocaris from the Burgess Shale
(Conway Morris, 1976, 1977; Gould, 1989). Amiskwia
sagittiformis (Fig. 11C) had a mollusc-like head and a
sagittiform body, at a time when neither the Mollusca
nor the Chaetognatha were established as phyla. Nectocaris pteryx (Fig. 11D) had a mollusc-like head and a
chordate body. Gould (1989) thought that the anterior
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D. I. WILLIAMSON
part of Nectocaris was arthropod-like, but I suggest
that the bivalve shell has its modern counterpart in
bivalve molluscs, and the eyes and tentacles have
modern counterparts in cephalopod molluscs. In the
mid-Cambrian, however, there were no molluscs or
classes of molluscs. As observed by Yochelson (1979),
‘“mollusc” is a zoological term, whereas “mollusc-like”
is a palaeontological term’.
The limits and definitions of taxonomic categories
are, to some extent, subjective. For example, different
B
A
C
D
Figure 11. Four mid-Cambrian species from the Burgess Shale of British Columbia. A, Laggania cambria (= Anomalocaris
nathorsti), ventral; B, Anomalocaris canadensis, ventral; C, Amiskwia sagittiformis; D, Nectocaris pteryx. Scale
bar = ∼200 mm (A, B), ∼5 mm (C, D). [A, B reproduced with permission from S M Gonn III (from ‘The Anomalocarid Bauplan’ http://www.geocities.com/goniagnostus/background3.html); C, D, from Marianne Collins in Gould, 1989.]
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HYBRIDIZATION IN EVOLUTION
authors have regarded the Crustacea as a class, a
superclass, a subphylum, and a phylum, and we may
question whether the terms phylum, class, order, etc.
in, say, arthropods are equivalent to those in other
major groups of animals, such as molluscs and echinoderms. These caveats are relevant to the following
suggestions on the origins of animal taxa.
Animals have evolved by Darwinian ‘descent with
modification’, by symbiogenesis and by hybridogenesis. Symbiogenesis was responsible, inter alia, for the
origin of protistans (Margulis, 1993) and for the acquisition of cnidae by cnidarians (Shostak & Kolluri,
1995). I claim that hybridogenesis was responsible not
only for the acquisition of larvae but also for the creation of the higher animal taxa. Concurrent chimeras
that resulted from Vendian, Cambrian or Ordovician
hybridizations between dissimilar animals were new
species in new potential phyla or classes. When such
species survived long enough, other species would
have evolved from them by Darwinian descent with
modification, and continued diversification would
have resulted in new genera and new families. I
believe that most species, genera, and families
evolved, and are still evolving, in this way. Phyla and
classes, on the other hand, were products of Vendian,
Cambrian, and Ordovician hybridizations between
disparate animals, when most species had spare
genome capacity and when specificity was evolving.
Hybridizations from the later Palaeozoic to the
present were responsible for the acquisition of larvae
by many animals. Some orders probably evolved by
descent with modification, others by hybridogenesis.
Fortey et al. (1996) believed that any explanation of
the Cambrian explosion requires ‘decoupling cladogenesis from morphological disparity’, and these
authors, like Valentine (2004), were seeking a cladistic
explanation for the origin of Cambrian phyla. Cladogenesis and all aspects of cladism are applicable only
to Darwinian evolution, which is within separate lines
of descent, or lineal. I claim, however, that the major
evolutionary events of the Cambrian explosion
resulted from hybridogenesis, a nonDarwinian evolutionary process, which, like symbiogenesis, entails
fusion of lineages, and is thus synlineal (Williamson,
1996). A corollary of symbiogenesis is that ‘the functions now performed by cell organelles are thought to
have evolved long before eukaryotic cells existed’
(Margulis, 1993). A corollary of larval transfer is that
‘the basic features of larvae are thought to have
evolved long before animals with larvae existed’ (Williamson, 2003). A corollary of component transfer, as
here discussed, is that the basic features of components of animals in different phyla are thought to have
evolved long before the respective phyla existed. Most
surviving animal phyla originated in the Cambrian
explosion, when simpler animals, each with its own
601
genome, hybridized to produce the first members of
these phyla. These simpler metazoans and the protistans that hybridized to produce them must have
originated earlier. This explains why Bromham et al.
(1998) concluded that molecular data are not compatible with the Cambrian explosion hypothesis as an
explanation of the origin of metazoan phyla. Molecular
data provide support for a period of Precambrian
diversification, as stated by Bromham et al. (1998) but
this was before the establishment of modern animal
phyla. Current molecular studies date the origins of
genes in recent animals. I submit that these genes
were present in the animals that hybridized to produce the first members of modern phyla, and further
mergers of genomes occurred in later hybridizations
that resulted in larval transfer.
ACKNOWLEDGEMENTS
I am grateful to Sam Gonn III for permission to use
his reconstructions in my Figure 11A, B, from ‘The
Anomalocarid Bauplan’ http://www.geocities.com/
goniagnostus/background3.html; to Enid Williamson
for drawing Figure 7E; and to Robert Higgins, Lynn
Margulis, Sonya Vickers, Robert Sternberg, Sebastian
Holmes, and Frank Ryan for assistance and helpful
discussions and suggestions.
REFERENCES
Abouheif E, Zardoya R, Meyer A. 1998. Limitations of
metazoan 18S rRNA sequence data: implications for reconstructing a phylogeny of the animal kingdom and inferring
the reality of the Cambrian explosion. Journal of Molecular
Evolution 47: 394–405.
Balfour FM. 1880–81. A treatise on comparative embryology. 2
volumes. London: Macmillan.
Boero F. 1980. Hebella parasitica (Cnidaria, Hydrozoa): a thecate polyp producing an anthomedusa. Marine Biology 59:
133–136.
Borradaile LA, Potts FA, Eastham LES, Saunders JT.
1935. The Invertebrata, 2nd edn. Cambridge: Cambridge
University Press.
Briggs DEG. 1983. Affinities and early evolution of the Crustacea: the evidence of the Cambrian fossils. In: Schram FR,
ed. Crustacean phylogeny. Rotterdam: Balkema, 1–28.
Bromham L, Rambaut A, Fortey R, Cooper A, Penny D.
1998. Testing the Cambrian explosion hypothesis by using a
molecular dating technique. Proceedings of the National
Academy of Sciences, USA 95: 12386–12389.
Collins D. 1996. The ‘evolution’ of Anomalocaris and its classification in the arthropod class. Dinocarida (nov.) and order
Radiodonta (nov.). Journal of Paleontology 70: 280–293.
Conway Morris S. 1976. Nectocaris pteryx, a new organism
from the Middle Cambrian Burgess Shale of British Columbia. Neues Jahrbuch für Geologie und Paläontologie, Monatshefte 1976: 705–713.
© 2006 The Linnean Society of London, Zoological Journal of the Linnean Society, 2006, 148, 585–602
602
D. I. WILLIAMSON
Conway Morris S. 1977. A redescription of the Middle
Cambrian worm Amiskwia sagittiformis Walcott from the
Burgess Shale of British Columbia. Palaeontologische
Zeitschrift 51: 271–287.
Conway Morris S. 2000. The Cambrian ‘explosion’: slow-fuse
or megatonnage? Proceedings of the National Academy of
Sciences, USA 97: 4426–4429.
Darwin C. 1859. On the origin of species by means of natural
selection or the preservation of favoured races in the struggle
for life. London: John Murray.
Fell HB. 1948. Echinoderm embryology and the origin of chordates. Biological Reviews. 23: 81–107.
Fell HB. 1963. The phylogeny of sea-stars. Philosophical
Transactions of the Royal Society of London B 246: 381–435.
Fell HB. 1968. Echinoderm ontogeny. In: Moore RC, ed. Treatise on invertebrate paleontology, Part 5, Echinodermata.
Lawrence: Geological Society of America and University of
Kansas Press, S60–S85.
Fortey R. 2000. Trilobite! Eyewitness to evolution. London:
HarperCollins.
Fortey RA, Briggs DEG, Wills MA. 1996. The Cambrian evolutionary ‘explosion’: decoupling cladogenesis from morphological disparity. Biological Journal of the Linnean Society
57: 13–33.
Gould SJ. 1989. Wonderful life. The Burgess Shale and the
nature of history. New York: W. W. Norton & Co. (1991 edition. London: Penguin).
Gurney R. 1942. Larvae of decapod Crustacea. London: Ray
Society.
Haeckel E. 1866. Generelle Morphologie der Organismen.
Algemeine Grundzügge der organischen Formen-Wissenschaft, mechanisch begründet durch die von Charles Darwin
Reformirte Descencendenz-Theorie. Berlin: Georg Reimer.
Hyman LH. 1959. The Invertebrates: smaller coelomate
groups.
Chaetognatha,
Hemichordata,
Pogonophora,
Phoronidia, Ectoprocta, Brachiopoda. The coelomate Bilateria, Vol. 5. New York: McGraw-Hill.
Margulis L. 1993. Symbiosis in cell evolution: microbial communities in archean and proterozoic eons. San Diego: W.H.
Freeman.
Migotto AE, de Andrade LP. 2000. The life cycle of Hebella
furax (Cnidaria: Hydrozoa): a link between a lafoeid hydroid
and a laodicid medusa. Journal of Natural History 34: 1871–
1888.
Müller KJ, Walossek D. 1986a. Arthropod larvae from the
Upper Cambrian of Sweden. Transactions of the Royal Society of Edinburgh, Earth Sciences 77: 157–179.
Müller KJ, Walossek D. 1986b. Martinssonia elongata gen.
et sp. n., a crustacean-like euarthropod from the Upper Cambrian Orsten of Sweden. Zoologica Scripta 15: 73–92.
Paul CRC. 1979. Early echinoderm radiation. In: House MR,
ed. The origin of major invertebrate groups. Systematics Association Special, Vol. 12. London: Academic Press, 443–481.
Schatt P, Féral J-P. 1996. Completely direct development of
Abatus cordatus, a brooding schizasterid (Echinodermata:
Echinoidea) from Kerguelen, with description of perigastrulation, a hypothetical new mode of gastrulation. Biological
Bulletin 190: 24–44.
Shostak S, Kolluri V. 1995. Symbiotic origin of cnidarian cnidocysts. Symbiosis 19: 1–19.
Smith AB. 1988. Fossil evidence for the relationships of extant
echinoderm classes and their times of divergence. In: Paul
CRC, Smith AB, eds. Echinoderm phylogeny and evolutionary biology. Oxford: Clarendon Press, 85–97.
Strathmann RR, Eernisse DJ. 1994. What molecular phylogenies tell us about the evolution of larval forms. American
Zoologist 34: 502–512.
Tattersall WM, Sheppard EM. 1934. Observations on the
bipinnaria of the asteroid genus Luidia. In: James Johnstone
memorial volume. Liverpool: Liverpool University Press,
35–61.
Valentine JW. 2004. On the origin of phyla. Chicago: University of Chicago Press.
Whittington HB. 1959. Ontogeny of Trilobita. In: Moore RC,
ed. Treatise on invertebrate paleontology. Part O, Arthropoda
1. Lawrence: Geological Society of America and University of
Kansas Press, O127–O145.
Whittington HB. 1974. Yohoia Walcott and Plenocaris n. gen.
Arthropoda from the Burgess. Shale, Middle Cambrian, British Columbia. Bulletin of the Geological Survey of Canada.
231: 1–21.
Whittington HB, Briggs DEG. 1982. A new conundrum from
the Middle Cambrian Burgess Shale. In: Mamet B, Copeland
MJ, eds. Proceedings of the third North American paleontological convention, Montreal, 2. Department of Geology: University of Montreal; Ottawa: Geological Survey of Canada,
573–575.
Williamson DI. 1988. Incongruous larvae and the origin of
some invertebrate life-histories. Progress in Oceanography
19: 87–116.
Williamson DI. 1991. Sequential chimeras. In: Tauber AI, ed.
Organism and the origin of self. Dordrecht: Kluwer, 299–
336.
Williamson DI. 1992. Larvae and evolution: toward a new
zoology. New York: Chapman. & Hall.
Williamson DI. 1996. Types of evolution. Journal of Natural
History 30: 1111–1112.
Williamson DI. 2001. Larval transfer and the origins of larvae. Zoological Journal of the Linnean Society 131: 111–122.
Williamson DI. 2002. Larval transfer in evolution. In: Syvanen M, Kado CI, eds. Horizontal gene transfer, 2nd edn.
New York: Academic Press, 395–410.
Williamson DI. 2003. The origins of larvae. Dordrecht:
Kluwer.
Williamson DI. in press. Larval transfer: experimental
hybrids. In: Margulis L, Asikainen CA, eds. Chimeras and
consciousness. Evolution of sensory systems. White River
Junction, Vermont: Chelsea Green Publishing Co.
Williamson DI, Rice AL. 1996. Larval evolution in the
Crustacea. Crustaceana. 69: 267–287.
Willmer PG. 1990. Invertebrate relationships: patterns in animal evolution. Cambridge: Cambridge University Press.
Yochelson EL. 1979. Early radiation of Mollusca and mollusclike groups. In: House MR, ed. The origin of major invertebrate groups. Systematics Association Special, Vol. 12.
London: Academic Press, 323–358.
© 2006 The Linnean Society of London, Zoological Journal of the Linnean Society, 2006, 148, 585–602