16 The Mollusca: Relationships and Patterns from Their First Half-Billion Years

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David R. Lindberg

Winston F. Ponder

Gerhard Haszprunar

252

Mollusks are bilaterally symmetrical eumetazoans that are

diverse in body form and size, ranging from giant squids more

than 20 m in length to adult body sizes of about 500 mm.

They are often considered to be the second largest phylum

next to Arthropoda, with about 200,000 living species, of

which about 75,000 living and 35,000 fossil have been

named, making them one of the better known invertebrate

groups. They also exhibit a great range of physiological, behavioral,

and ecological adaptations. Mollusks have an excellent

fossil record extending back some 560 million years

to the early Cambrian, and perhaps into the Precambrian as

well. Three major classes, Gastropoda (snails, slugs, limpets),

Bivalvia (scallops, clams, oysters, mussels) and Cephalopoda

(squid, cuttlefish, octopuses, nautilus), are recognized, as well

as four or five minor living classes [Aplacophora (spicule

worms)—which are often divided into two separate classes,

Polyplacophora (chitons), Scaphopoda (tusk shells), and

Monoplacophora (a small group of deep sea limpets with a

long fossil history)]. A few extinct groups often treated as

classes are also recognized.

The majority of mollusks are marine, but large numbers

also occupy freshwater and terrestrial habitats. They are extremely

diverse in their food habits, ranging from grazers and

browsers on many different biotic substrates to suspension

feeders, predators, and parasites. Many are economically

important as food, cultural objects, hosts for human parasites,

or pests. Many nonmarine taxa are also in jeopardy as

a result of human activities. Despite only a small fraction of

the world’s nonmarine molluscan faunas being adequately

assessed, there are more recorded extinctions of these mollusks

than of birds and mammals combined (Ponder 1997,

Killeen et al. 1998, Seddon 1998). In addition, alien species

are resulting in the homogenization of many previously

unique biotas, especially on islands (Cowie 2002).

Some common morphological features enable Mollusca

to be characterized as a monophyletic group. These include

having the body, which typically has a head, foot, and visceral

mass, covered with a pallium or mantle that typically

secretes the shell (or, more rarely, spicules), although this is

secondarily lost in some groups (e.g., slugs, octopuses). Typically,

there are one or more pairs of gills (ctenidia), which

lie in a posterior pallial (i.e., mantle) cavity or in a posterolateral

groove surrounding the foot, into which the kidneys,

gonads, and anus open and which also contains a pair of

sensory osphradia. The buccal cavity contains a radula—a

ribbon of teeth supported by a muscular odontophore (lost

in bivalves). There is a ventral foot used in locomotion using

muscular waves and/or cilia in combination with mucus.

They are coelomate, although the coelom is small and represented

by the kidneys, gonads, and pericardium, the main

body cavity being a haemocoel. They lack segmentation and

have spiral cleavage. Trochophore and/or veliger larvae are

found in many aquatic taxa, but direct development is also

common.

The earliest undoubted mollusks are found in the early

Cambrian (~560 million years ago), when several major groups

The Mollusca: Relationships and Patterns from Their First Half-Billion Years 253

(gastropods, bivalves, monoplacophorans, and rostroconchs)

appear. Cephalopods are found from the Middle Cambrian,

polyplacophorans from the Late Cambrian, and scaphopods

from the Middle Ordovician. Studies on molluscan evolution

are able to use this rich fossil diversity and can be particularly

illuminating when combined with morphological,

ultrastructural, embryological, and molecular studies on taxa

from the Recent period. Studies on the genetics, diversity,

phylogeny, and ecology of mollusks have provided important

insights into evolutionary biology, biogeography, and

ecology in general.

Phylogenetic Scenarios and Hypotheses

There have been two traditions for placing Mollusca on the

Tree of Life—one paleontological (using fossils) and the other

neontological (using living taxa). These traditions extend to

varying degrees into the subclades that make up Mollusca.

Every so often workers unify these traditions with varying

degrees of success. An early example was Dall’s (1893) noting

of the symmetry of the adductor scars of Paleozoic

monoplacophoran fossils and that they “paralleled in some

particulars the organization of some of the Chitons of that

ancient time.” It was 45 years before the same suggestion

was made by Wenz (1938–1944), and another 19 years

before the discovery of living monoplacophorans (Lemche

and Wingstrand 1959) confirmed Dall’s insight into the

nontorted state of these animals. Like Dall, Knight (1952)

used observations on living gastropods and applied them to

fossil gastropod morphologies, creating new evolutionary

scenarios and generating a renaissance in thinking about

gastropod evolution.

However, by the late 1960s, interest in systematics was

waning, and a new generation of paleontologists, including

S. Gould, D. Raup, S. Stanley, J. Valentine, and G. Vermeij,

moved the field to a more theoretical position from which

to evaluate patterns and processes of taxic evolution. For many

of these workers, Mollusca was the taxon of choice because of

its diversity and record from deep time. Systematics continued,

especially on Paleozoic taxa, where E. Yochelson, J. Pojecta,

B. Runnegar, S. Bengsten, J. Peel, and their colleagues were

discovering new major lineages and setting the stage for reinterpreting

previous findings (see Runnegar 1996). New

evolutionary scenarios for patterns seen in the fossil record

were proposed, and molluscan groups were often used to test

many of these new theories, including patterns of heterochrony

and punctuated equilibrium, theoretical morphospaces,

and community and phyletic patterns of ecological

interactions. Such an integrated approach quickly brought

molluscan evolutionary biology into a much more paleontological

framework. A notable exception during this period

was the work of L. Salvini-Plawen, who continued to study

molluscan origins from an almost exclusively neontological

position (Salvini-Plawen 1972, 1980). Molecular data have

recently joined these two more traditional molluscan data sets

and—as would be predicted under Murphy’s Law—currently

falsifies neither the paleontological nor the neontological

views.

To ultimately render robust hypotheses of molluscan

origins and relationships, all of these data sets need to be

compared, combined, parsed, and analyzed. It is likely that

too much time has passed since the divergences and/or the

time span is too short to preserve that perfect phylogenetic

marker. This problem has been recognized and examined in

paleontological studies (e.g., Wagner 2001), in morphological

studies (e.g., Lindberg and Ponder 1996, Ponder and

Lindberg 1996, 1997), and more recently in molecular studies

(e.g., Giribet 2002).

What Makes a Spiralian Taxon a Mollusk?

Currently there is no consensus as to the identity of the sister

taxon of Mollusca. Contenders include Brachiopoda, suggested

by the 28S data set (Mallat and Winchell 2001). Haszprunar

(1996; fig. 16.1) has suggested the kamptozoans based on

developmental data (body wall cuticle, blood sinuses) and

larval characters (cuticle, ciliary gliding sole with pedal gland).

However, confirmation of these details is needed because only

one description of a kamptozoan larva has appeared in the

literature (Nielsen 1971). Sipuncula has been suggested by

Scheltema (1993, 1996) based on developmental and larval

characters. Traditionally, Annelida have been considered the

sister taxon of Mollusca by most workers and in some text

books (Brusca and Brusca 2002). The mollusks and annelids

share several characters, including the trochophore larvae,

anteriorly positioned ferrous oxide structures as teeth and jaws,

and a cross configuration of micromeres during early development.

However, the Arthropoda–Annelida–Mollusca triad,

which dominated invertebrate classification for more than 75

years, was ultimately overturned by molecular and other data,

revealing that the supposed relationship of these three taxa

(based on the supposed shared “similarity” of body segmentation)

was actually convergent.

Ghiselin (1988) and Winnepenninckx et al. (1994, 1995)

provide some of the earliest analyses of small subunit (18S)

ribosomal DNA (rDNA), and for many years this served as

the basis for many molluscan outgroup comparisons. These

and other studies suggested that mollusks reside among the

lophotrochozoan taxa (mollusks, annelids, brachiopods,

bryozoans, and phoronids; Halanych et al. 1995; fig. 16.2).

However, the relative branching of these taxa is not clearly

delineated by 18S data (Medina and Collins 2003). Zrzavэ

et al. (1998), using a combined analysis of 18S data and

morphology, suggested that the sipunculids were the sister

taxon of the mollusks. However, Boore and Staton (2002),

using partial mitochondrial DNA (mtDNA) gene order data,

suggested the sipunculids are actually more closely related

to annelids rather than to mollusks. In addition, Mallat and

254 The Relationships of Animals: Lophotrochozoans

Winchell (2001) suggested that brachiopods and/or phoronids

may be the molluscan sister group based on their analyses

of complete 28S sequences. Surprisingly, there is little

molecular evidence to test the hypothesis of Annelida as the

sister taxa of Mollusca, although morphological and developmental

evidence of this relationship has been long-standing

(Ghiselin 1988). mtDNA gene order data may be important

in understanding the position of Mollusca on the Tree of Life

(Medina and Collins 2003) because, unlike many other phyla,

all the molluscan mtDNA genomes examined so far show

major rearrangements (Boore and Brown 1994, Boore 1999).

However, as a cautionary note, Adoutte et al. (2000) have

suggested that the inability to clearly identify a sister taxon

of Mollusca may result from the burst of rapid speciation in

the Cambrian within the three major bilaterian lineages.

Any of the outgroups discussed above would suggest a

worm bauplan for the last common ancestor of the molluscan

taxa. Whether or not the worm was covered with a cuticle,

spicules, or shell cannot be determined because hardening

of the ectoderm is present in several outgroups, including

the brachiopods (both calcium carbonate and calcium phosphate

shells), annelids (fibrous cuticle, secondary calcium

carbonate tubes), and members of Kamptozoa (chitinous

cuticle). A crossed lamella-like microstructure in the molluscan

shell appears to be plesiomorphic by outgroup comparisons

(hyoliths); foliated structures are present in both

mollusks and brachiopods and, along with nacre, have been

independently derived in bivalve and gastropod mollusks

(Hedegaard and D. R. Lindberg, unpubl. obs.).

Molluscan Characters, Plesiomorphy,

Apomorphy, and Homoplasy

The presence of a pericardium—a coleomic cavity that encloses

the heart and performs ultrafiltration in several taxa

(Andrews 1988, Meyhoefer and Morse 1996)—is a synapomorphy

of Mollusca. Addition of repeated structures from

posterior to anterior and a radula and a tripartite mantle edge

divisible into outer, middle, and inner folds are also molluscan

synapomorphies [see Haszprunar (1996) for additional

ultrastructure characters].

Most mollusks have a space between the mantle and the

side of the foot that forms the pallial (or mantle) groove.

Typically, the groove deepens posteriorly and forms a cavity

that contains a pair of gills or ctenidia, as well as openings of

the rectum, paired renal organs, and gonads from the dorsal

visceral mass. Although the molluscan pallial cavity has long

been considered a single defining system, character transformations

of many of the individual components that make up

the pallial cavity system can be problematic (Lindberg and

Ponder 2001). For example, a single pair of ctenidia is common

in hypothetical ancestors of the major clades, but its

distribution on the tree is not informative, and its current

function in many groups is likely autapomorphic. Members

of Mollusca, like other lophotrochozoans, have gills that have

both respiration and ventilation functions. In several taxa

(within and outside mollusks), filter feeding is a third part

of the repertoire of gills, and they also play a role in brooding

larvae in several taxa.

Lindberg and Ponder (2001) argued that phyletic size

increase in Gastropoda increased selective pressure for increased

efficiency of the gills and the separation of ventilation

and respiration functions. Suggestions of the same conflict

are present in the other molluscan taxa and well illustrate the

nested sets of parallel evolution present throughout the molluscan

tree.

For example, the Polyplacophora increase both respiratory

and ventilation surfaces simultaneously by adding gills

in serial repetition from posterior to anterior as phyletic size

increases (Lindberg 1985). In Monoplacophora, ventilation

currents appear to be generated by the ctenidia (added in

Figures 16.1 and 16.2. Phylogenetic

relationships of putative

molluscan outgroups. 16.1.

Morphological data (Haszprunar

1996). 16.2. Molecular data

(18S rDNA; Halanych et al.

1995).

Lobatocerebrum

Nemertinea

Kamptozoa

Mollusca

Sipunculida

Echiurida

Polychaeta

Clitellata

Echinoderm

Bryozoan

Inarticulate

Chiton

Bivalve

Polychaete

Articulate

Phoronid

Crustacean

Cheilicerate

Cephalochordate

Vertebrate

Anthozoan

Scyphozoan

]Mollusca

16.1 Haszprunar (1996) 16.2 Halaynch et al. (1995)

The Mollusca: Relationships and Patterns from Their First Half-Billion Years 255

serial repetition from posterior to anterior), and the pallial

groove serves as the respiratory surface (Lindberg and Ponder

1996, Haszprunar and Schaefer 1997a). In Bivalvia, the

hypothetical ancestral states are inferred from the depositfeeding

protobranchs where the paired gills are used as ventilators

and respirators alone within a spacious pallial cavity.

These structures are probably reliable analogues of the likely

progenitors of the larger, more complex gills of other bivalves

that are highly modified for suspension feeding. In Cephalopoda,

Nautilus alone has two pairs of ctenidia; the remainder,

one pair. Ventilation currents are produced by muscular

contractions of the mantle or funnel (Ghiretti 1966), and the

gills are used solely in respiration. The circulatory system is

closed with the ctenidia, in many living cephalopods, having

auxiliary hearts that increase the rate of blood passing

through the gills in these large, very active animals. Scaphopods

lack gills, but the elongate pallial cavity is large, and

strong bands of cilia drive water circulation along with regular

muscular contractions. Lastly, the plesiomorphic state of

gastropods was paired gills with a small shallow pallial cavity

(Lindberg and Ponder 2001), although this configuration

is highly modified in most taxa.

In the chaetodermomorphs, paired gills are present in a

small posterior pallial cavity; in the nonburrowing Neomenimorpha,

only gill folds are present around a rudimentary

posterior pallial cavity. Thus, whether members of the

aplacophoran (grade or clade) represent the clade Aculifera,

or are the stem taxa of Mollusca, they do not assist in polarizing

the outgroup node for the plesiomorphic character

states of the conchiferian ctenidium (primary gill). The inability

to polarize gill character states continues within

Conchifera. Thus, the only character states for the gill of the

molluscan common ancestor that can be strongly argued are

filament shape and ventilation (table 16.1). Although there

are certainly majority rule candidates among the other gill

characters (e.g., paired ctenidia, ctenidia + pallial cavity respiration),

none of the remaining character states are supported

by the duplet rule (Maddison et al. 1984) at any node

in previously reported phylogenies (figs. 16.3–16.6). There

are other majority rule characters that are often cited as

molluscan ancestral states, including the presence of a head

region (lacking tentacles and eyes), a ventral muscular foot,

a dorsal visceral mass, and an enveloping mantle (= pallium)

that secretes spicules and/or the shell, but these characters,

like the gill characters, cannot be unequivocally confirmed

by outgroup analysis. This inability to estimate character

polarity is a common outcome throughout the molluscan tree

(for Gastropoda, see Ponder and Lindberg 1997).

The digestive system of mollusks follows a common pattern,

although in some aplacophoran and conchiferan groups

(cephalopods, bivalves, and some gastropods) it is highly

modified. The molluscan digestive system is autapomorphic

to potential outgroups and consists of numerous glands and

sacs associated with the buccal chamber. The mouth opens

to a buccal cavity that typically contains paired jaws and a

muscular odontophore that typically bears the radula and a

pair of salivary glands. All of these structures, other than the

mouth, are lost in bivalves. An esophagus, sometimes with

glandular pouches, opens to a typically complex stomach

where a large pair of digestive glands also open. Ciliary tracts

sort food particles from the waste material in the stomach,

and digestion occurs in the digestive gland. Waste is moved

to the intestinal part of the stomach that typically starts as a

style sac in which the waste string is rotated and bound with

mucus before being passed into the intestine proper. In most

bivalves and some gastropods, a crystalline style, a rotating

rod of muco-protein that releases digestive enzymes, lies in

the style sac. The hindgut or intestine is often long and looped

or coiled. Fecal material is released through the anus that

typically lies within the pallial cavity.

All mollusks other than cephalopods (as noted above)

have an open circulatory system with blood sinuses, a heart,

blood vessels, and respiratory pigment, usually hemocyanin.

The heart is enclosed within the pericardium and has multiple

(usually two, one in many gastropods) auricles and

a single ventricle. Cephalopods have a closed system with

arteries and veins. Gas exchange is via gills, lungs, or the

body surface. Excretion takes place by means of kidneys

(nephridia) that excrete waste into the pallial cavity. The

excretory system is paired and connected to the pericardium

as well as the gonads in some taxa. The gonads are also paired

but can be fused into a single structure (Polyplacophora) or

reduced to a single organ (Gastropoda and Scaphopoda).

Separate gonoducts are present in some taxa, and in other

taxa the gonads empty into the kidneys. These connected,

mesodermal structures (pericardium, kidneys, and gonads)

likely represent the coelom of Mollusca.

Most mollusks are dioecious (separate sexes); some, monoecious

(hermaphroditic). Some groups have internal fertilization

and produce various forms of jelly or capsule-covered

eggs that contain the embryo for at least part of its development;

others release their gametes into the water column and

their development is entirely pelagic, passing through both trochophore

and veliger stages. Some planktonic larvae feed on

the plankton and other suspended particles (planktotrophic);

others feed on nutrients stored in the egg (lecithotrophic).

Some species have direct development, with juveniles emerging

from the egg capsule or from a brood pouch within the

parent. Internal fertilizing taxa may transfer sperm during

copulation involving a penis or, as in cephalopods and some

gastropods, by transferring spermatophores—packets of

sperm.

The nervous system consists of four main paired centers—

cerebral, visceral, pedal, and pleural ganglia. They are

connected by commissures; in the plesiomorphic condition

the paired pedal nerve cords extend ladderlike through the

foot. Sensory and nervous systems are concentrated in the

head region, especially in gastropods and cephalopods.

Highly specialized sense organs are on the head (eyes, tactile

organs such as tentacles), as well as statocysts for balance

256 The Relationships of Animals: Lophotrochozoans

Table 16.1

Assumed Plesiomorphic Character States for Respiratory Structures in the Molluscan Pallial Cavity.

Character Polyplacophora Neomeniomorpha Chaetodermomorpha Monoplacophora Bivalvia Scaphopoda Cephalopoda Gastropoda

Pallial groove Long, narrow Absent Shallow posterior Long, narrow Large, Large, elongate, Large ventral Shallow (deep in

groove around foot embayment groove around surrounds extends length embayment advanced taxa),

foot entire of animal anterior embayment

animal inside shell

Ctenidia 5–60 pairs Absent 1 pair 3–6 pairs 1 pair Absent Nautilus, 1 pair (reduced to

2 pairs; all one ctenidium or

others, 1 pair lost in most

gastropods)

Skeletal rods Absent NA Absent Absent Present NA Present Absent

(efferent) (afferent)

Filament shape Semicircular NA Semicircular Semicircular Semicircular NA Semicircular Semicircular

(triangular to

elongate in most

gastropods

Ventilation Ctenidia NA Ctenidia Ctenidia Ctenidia Ciliary bands, Musculature Ctenidia

musculature

Respiration Ctenidia + pallial Subcutaneous Ctenidia + pallial Pallial cavity Ctenidia + Pallial cavity Ctenidia Ctenidia + pallial

cavity? cavity? Pallial cavity cavity

From Haszprunar (1988) and Lindberg and Ponder (2001).

The Mollusca: Relationships and Patterns from Their First Half-Billion Years 257

and chemosensory osphradia, a pair of specialized patches

in the pallial cavity. Light receptors are found on the dorsal

surface of some mollusks (e.g., chitons) and on the mantle

edge, particularly in some bivalves (where they may be structurally

complex and eyelike). Many gastropods have small

cephalic eyes, which are rather complex in some groups. Most

living cephalopods have large, complex eyes that parallel

those of vertebrates.

During development, mollusks are one of several invertebrate

phyla that undergo spiral cleavage. Embryological studies

show that they have true coelomic cavities formed by the

splitting of embryonic mesodermal masses (schizocoely) and

that they have protostomous development (mouth develops

before the anus); these characteristics are shared with several

other phyla that are grouped as Eutrochozoa within Spiralia.

Many mollusks pass through free-swimming larval stages

called trochophore and veliger larvae. The trochophore larva,

characterized by its apical tuft of cilia and ciliated bands, is

found in primitive gastropods and many bivalves, as well as

aplacophorans, scaphopods, and chitons. Similar larvae are

also found in other marine invertebrate phyla, including

Annelida, Sipuncula, and Entroprocta. Veliger larvae are

characteristic of gastropods and bivalves and have a bilobed,

ciliated swimming organ known as the velum that, in feeding

larvae, also collects food particles from the water.

The molluscan body plan has been substantially modified,

both among and within groups (table 16.2). Diversification

appears to have occurred early in the history of

Mollusca, but there has been surprisingly little change in

some groups. For example, the shells of some Late Cambrian

monoplacophorans are almost identical to those of living taxa

despite 450 million years of evolution. Other examples of

little change to molluscan body plan include protobranch

bivalves, nautiloids, and scaphopods.

Figures 16.3–16.6. Phylogenetic

relationships of living

molluscan classes based on

morphological data. 16.3.

Runnegar (1996), with extinct

taxa removed. 16.4. Salvini-

Plawen and Steiner (1996).

16.5. Waller (1998). 16.6.

Haszprunar (2000).

Polyplacophora

Monoplacophora

Cephalopoda

Gastropoda

Scaphopoda

Bivalvia

Caudofoveata

Solengastres

Caudofoveata

Solengastres

Polyplacophora

Monoplacophora

Gastropoda

Cephalopoda

Scaphopoda

Bivalvia

Polyplacophora

Caudofoveata

Solengastres

Monoplacophora

Bivalvia

Gastropoda

Cephalopoda

Scaphopoda

Solengastres

Caudofoveata

Polyplacophora

Monoplacophora

Bivalvia

Scaphopoda

Gastropoda

Cephalopoda

16.3 Runnegar (1996) 16.4 Salvini-Plawen and Steiner (1996)

16.5 Waller (1998) 16.6 Haszprunar (2000)

258 The Relationships of Animals: Lophotrochozoans

Fossil History

Mollusca include some of the oldest metazoans known. Late

Precambrian rocks of southern Australia and the White Sea

region in northern Russia contain bilaterally symmetrical,

benthic animals with a univalved shell (Kimberella) that resembles

those of mollusks in some respects. The earliest

unequivocal mollusks are helcionelloid mollusks that date

from Late Vendian rocks (Gubanov and Peel 2000). In the

Early Cambrian the Coeloscleritophora are also present. Most

of the familiar groups, including gastropods, bivalves, monoplacophorans,

and rostroconchs, all date from the Early

Cambrian, whereas cephalopods are first found in the Middle

Cambrian, polyplacophorans in the Late Cambrian, and

Scaphopoda in the Middle Ordovician (Wen 1990). Most of

these taxa tend to be small (<10 mm in length; Runnegar

1983). The Late Vendian–Early Cambrian taxa bear little

resemblance to the Cambrian–Ordovician lineages (most of

which remain extant today). After their initial appearances,

taxonomic diversity tends to remain low until the Ordovician,

when gastropods, bivalves, and cephalopods show

strong increases in diversity. For bivalves and gastropods,

this diversification increases throughout the Phanerozoic,

with relatively small losses at the end-Permian and end-Cretaceous

extinction events. Cephalopod diversity is much

more variable through the Phanerozoic, whereas the remaining

groups (monoplacophorans, rostroconchs, polyplacophorans,

and scaphopods) maintain low diversity over the

entire Phanerozoic or became extinct (Sepkoski and Hulver

1985).

There is a diversity of views on whether many of the

Cambrian univalved mollusks should be interpreted as either

gastropods or untorted taxa, and substantially divergent

phylogenetic scenarios can result. In the most recent scheme,

Parkhaev (2002) has proposed a new gastropod subclass

(Archaeobranchia) to contain taxa he considered to be torted

and, therefore, gastropods. His action is based in part by the

allocation of Helcionellacea to Gastropoda by Knight and

Yochelson (1958). Most of the taxa allocated to the Archaeobranchia

have also been treated as monoplacophorans (e.g.,

Runnegar 1983, Runnegar and Pojeta 1985) or as a separate

class (Helcionelloida; Peel and Yockelson 1987, Peel 1991).

However, when these controversial extinct taxa are removed

from paleontological analysis of molluscan relationships,

the resulting trees are often remarkably similar to current

phylogenetic schemes based on living taxa (Runnegar 1996;

fig. 16.3).

Habitats and Habits

Mollusks occur in almost every habitat found on Earth, where

they are often the more conspicuous organisms and sometimes

predominant (table 16.3). Although most are found in

the marine environment, where they extend from the supralittoral

to the deepest oceans, several major gastropod clades

predominantly live in freshwater or terrestrial habitats. Marine

diversity is highest nearshore and becomes reduced as

depth increases beyond the shelf slope. Like many other

organisms, marine mollusks reach their highest diversity in

the tropical western Pacific and decrease in diversity toward

the poles. Only one comprehensive study on molluscan diversity

has been carried out in the tropical western Pacific,

where around 3000 species have been found within a single

site in coral reef habitat in New Caledonia (Bouchet et al.

2002). In terrestrial communities, gastropods can achieve

reasonably high diversity and abundance: as many as 95

species may coexist in a single square kilometer of Cameroon

Table 16.2

Morphological Diversity of Living Adult Members of the Major Molluscan Clades.

Anopedal Number

Taxon flexure Wormlike Shell absent of shells Coiled Slug Limpets Fishlike

Polyplacophora 8

Neomeniomorpha ** ** NA

Chaetodermomorpha ** ** NA

Monoplacophora 1 **

Bivalvia * 2

Scaphopoda * 1

Cephalopoda * * 1 (*) **

Gastropoda * (*) * 1 (2) * * * (*)

Patellogastropoda * 1 **

Cocculinida * 1

Vetigastropoda * (*) 1 ** *

Neritopsina * (*) 1 ** (*) (*)

Caenogastropoda * (*) (*) 1 ** (*) (*) (*)

Heterobranchia * (*) * 1 (2) ** ** (*) (*)

** = predominant, * = well represented, (*) = rare.

Data compiled by D. R. Lindberg and W. F. Ponder.

The Mollusca: Relationships and Patterns from Their First Half-Billion Years 259

rainforest (de Winter and Gittenberger 1998), and abundance

in leaf litter can exceed more than 500 individuals in

four liters of litter. Abundance and diversity for some groups

can also be higher in temperate communities than in tropical

settings. In freshwater communities, where both gastropods

and bivalves co-occur, species diversity can also be high.

Historically, in rivers of the southeastern United States,

more than 100 species of mollusks (97 bivalves and a minimum

of 12 different species of gastropods) were found on

a single mussel shoal (P. J. Johnson, pers. comm.), and

abundances of native freshwater unionid bivalves can approach

300 clams/m2 in this same region (Johnson and

Brown 2000). But these numbers pale compared with the

introduced zebra mussel (Dreissena polymorpha), which can

exceed more than 30,000 individuals/m2 in North America

(Dermott and Munawar 1993).

Marine mollusks occur on a large variety of substrates,

including rocky shores, coral reefs, mud flats, and sandy

beaches. Gastropods and chitons are characteristic of these

hard substrates, and bivalves are commonly associated with

softer substrates, where they burrow into the sediment.

However, there are many exceptions: the largest living bivalve,

Tridacna gigas, nestles on coral reefs, many bivalves

(e.g., mussels, oysters) are attached to hard substrates; microscopic

gastropods live interstitially between sand grains,

and some are stygobionts.

The adoption of different feeding habits appears to have

had a profound influence on molluscan diversification

(table 16.4). The change from grazing to other forms of food

acquisition is one of the major features in the adaptive radiation

of the group (Ponder and Lindberg 1997, Vermeij

and Lindberg 2000). Based on our current understanding of

relationships (figs. 16.3–16.6), the earliest mollusks were

carnivores or grazed on encrusting animals and detritus. Such

feeding may have been selective or indiscriminate and will

have encompassed algal, diatom, or cyanobacterial films and

mats, or encrusting colonial animals. Truly herbivorous grazers

are relatively rare and are limited to some polyplacophorans

and a few gastropod groups (Vermeij and Lindberg

2000). Most chaetodermomorph aplacophorans, monoplacophorans,

and scaphopods feed on protists and/or bacteria,

whereas neomeniomorph aplacophorans graze on

cnidarians. Cephalopods are mainly active predators as are

some gastropods, whereas a few chitons and septibranch

bivalves capture microcrustaceans. Most bivalves are either

suspension or deposit feeders that indiscriminately take in

particles but then elaborately sort them based on size and

weight.

Cephalopods are typically active carnivores specialized

on mobile prey such as fish, crustaceans, and other cephalopods.

Because they are so abundant in pelagic systems, cephalopods

are often important food sources for larger fishes,

marine mammals, and seabirds. In the gastropods, members

of Janthinidae are planktic pelagic carnivores feeding on

cnidarians, whereas the heteropods (Caenogastropoda) and

the gymnosomes (Opisthobranchia), like the cephalopods,

are active swimmers in search of prey. These taxa spend their

entire lives in the water column feeding on other mollusks

(including small cephalopods), crustaceans, and even fishes.

In addition to these more typical trophic strategies and interactions,

some are endo- or ectoparastic, and the glochidium

larvae of freshwater unionid bivalves parasitize fish and

amphibians, although the adults are free living (see below).

Molluscan groups are ubiquitous and diverse in marine

habitats, but only the bivalves and gastropods have invaded

freshwater habitats, and only gastropods have invaded terrestrial

ones. In nonmarine habitats, gastropods can be found

in the wettest environments of tropical rainforests and in the

Table 16.3

Habitats Occupied by Living Adult Members of the Major Molluscan Clades.

Marine benthic Terrestrial

Taxon Shallow Deep column Estuarine Freshwater Damp Arid

Polyplacophora ** (*)

Neomeniomorpha (*) **

Chaetodermomorpha * **

Monoplacophora **

Bivalvia ** * (*) * *

Scaphopoda ** *

Cephalopoda * * ** (*)

Gastropoda ** * (*) * * * *

Patellogastropoda ** (*) (*)

Cocculinida **

Vetigastropoda ** ** *

Neritopsina ** * * * *

Caenogastropoda ** * * * * * (*)

Heterobranchia ** * * * * ** *

** = predominant, * = well represented, (*) = rare.

Data compiled by D. R. Lindberg and W. F. Ponder.

Water

260 The Relationships of Animals: Lophotrochozoans

driest deserts, where their annual activity patterns may be

measured in hours. Some live below ground in the lightless

world of aquifers and caves, and others interstitially in

groundwater (stygobionts). The major terrestrial clade is the

pulmonate gastropods, which originated at least by the Carboniferous

period (Solem and Yochelson 1979), but other

taxa that have nonmarine groups such as the neritopsines

and caenogastropods are likely Devonian/Silurian in origin

(Frэda 2001, Frэda and Blodgett 2001, Wagner 2001). Often

the terrestrial groups are among the most basal of the

extant taxa in the clade. For example, in both Neritopsina

and Caenogastropoda, nonmarine taxa are thought to be

more basal than marine members of these groups (Ponder

and Lindberg 1997). These patterns could result from competition

among sister taxa and the relegation of one taxon to

a unique habitat while the other diversified in the ancestral

setting.

Shell morphology is often thought to be correlated with

lifestyle and habitat, and some substantial changes in body

form are clearly associated with major adaptive changes.

Frequently, however, morphology is not readily correlated

with habitat, and similar shell morphologies do not necessarily

indicate similar habits or habitats. For example, limpet

taxa occur on wave-swept platforms, on various substrates

in the deep sea, at hot vents, in fast-flowing rivers, in quiet

lakes and ponds, and as parasites on oysters and starfish. It

is often suggested that strong wave action selects for limpet

morphology, but it is obvious from their known habitat distributions

that mollusks with limpet-shaped shells do very

well in a wide range of habitats (Ponder and Lindberg 1997).

Suspension feeding is characteristic of most bivalves but

has also evolved in some gastropods such as the vetigastropod

Umbonium and several caenogastropods (e.g., turritellids and

calyptraeids) and in the pelagic heterobranch group Thecosomata.

Some groups with carnivorous diets have undergone

what appear to be true, explosive adaptive radiations (e.g.,

the Neogastropoda). Others that are food specialists such as

the neomeniomorph aplacophorans and scaphopods have

low diversity and abundance.

Several groups of bivalves, including Lucinidae and

Solemyidae, have developed symbiotic relationships with

bacteria that live in their modified gills and reduce or even

eliminate the need for the uptake of alternative food supplies.

The giant clams (or tridacnids), a number of other bivalves,

and a few opisthobranch gastropods have symbiotic relationships

with zooxanthellae embedded in their tissues.

Large concentrations of gastropods and bivalves are

found at hydrothermal vents in the deep sea. Living in these

or other dysoxic habitats appears to be a plesiomorphic condition

for Mollusca and several outgroups. For example, the

fauna of Paleozoic hydrothermal vent communities includes

the molluscan groups Bivalvia, Monoplacophora, and Gastropoda

as well as the outgroups Brachiopoda and Annelida

(Little et al. 1997).

Outline of Major Groups

How important is the molluscan branch on the Tree of Life?

Molluscan history is filled with incredible diversifications.

Numerical abundance and diversification of living species

have been previously referred to, but the total number of living

species likely represents less than 5% of the total molluscan

diversity that has ever lived. Many of the major lineages

of the gastropods and bivalves survived the great extinctions.

Some other major groups of mollusks did not, such as the

ammonites, which did not survive the Cretaceous–Tertiary

extinction. Taxa with high taxonomic diversity are often

Table 16.4

Feeding Types in the Major Molluscan Clades.

Grazing

Taxon Detritivory Macroherbivory carnivory Microcarnivory Hunting Parasitic Suspension

Polyplacophora * ** (*)

Neomeniomorpha **

Chaetodermomorpha **

Monoplacophora **

Bivalvia * (*) **

Scaphopoda **

Cephalopoda ** ?

Gastropoda ** * ** * * (*) (*)

Patellogastropoda (*) **

Cocculinida **

Vetigastropoda ** * ** (*)

Neritopsina ** **

Caenogastropoda ** * * * * (*) (*)

Heterobranchia * * ** * ** (*) (*)

** = predominant, * = well represented, (*) = rare.

Data from D. R. Lindberg and W. F. Ponder.

The Mollusca: Relationships and Patterns from Their First Half-Billion Years 261

thought of as evolutionarily successful and therefore important

in evolutionary studies. However, more than just numerical

dominance should be considered in laying out an

evolutionary research program. For example, although

beetles, amphibians, and mollusks are numerically and ecologically

diverse, the first two groups are rare in the fossil

record compared with Mollusca. Although patterns of current

diversity are intriguing, the degree of resolution of these

patterns and the ability to deduce and test potential processes

responsible for them through time are of great importance

in diversity studies. Mollusca is one of the few groups that

provides adequate data in this historical context.

As this volume attests, the state of our knowledge of

metazoan phylogeny and taxa (including the Mollusca), and

the wealth of new data that are now appearing from molecular,

developmental, morphological, and paleontological

work, will cause any classification proposed here to become

rapidly outdated. Several traditional classifications are available

in the references cited below. However, few are based

on hypotheses of relationships, but are instead based on

overall similarity and ad hoc scenarios of evolution.

Classifications based solely on morphology have been

especially problematic, and much of this confusion has resulted

from problematic taxa such as the aplacophorans,

scaphopods, and bivalves, where possible reduction and loss

of organs or other secondary simplification have produced

morphologies that may be argued as either primitive or highly

derived. Many of classification have also focused exclusively

on the morphology of living taxa and have ignored potential,

fossil members of Mollusca. If extinct fossil taxa are included

in evolutionary scenarios, they are typically limited to distinctive

clades such as Rostroconchia and Bellerophonta. Other

more problematic extinct taxa (e.g., hyoliths) are systematically

ignored, arbitrarily excluded from Mollusca without

analysis, or shoe-horned into extant groups.

In some classifications (figs. 16.3, 16.4), the higher taxa

have been treated as classes and arranged into several groupings,

for example, the Conchifera (Gastropoda + Monoplacophora

+ Bivalvia + Scaphopoda + Cephalopoda), the

Visceroconcha (Gastropoda + Cephalopoda) and the Diasoma

(= Loboconcha; Bivalvia + Scaphopoda). In these classifications,

the sister taxa of Mollusca have included Annelida,

Lophophorates, and Kamptozoa (figs. 16.1, 16.2), and within

Mollusca, both Polyplacophora and aplacophoran taxa have

been argued as the most primitive taxa and therefore the

outgroup to all Conchifera (figs. 16.3–16.6).

Most classifications have also assumed a single cladogenetic

event in the origin of the Conchifera from the supposedly

more primitive placophoran groups. Alternative hypothesis

have derived the conchiferans in an unresolved polytomy from

a hypothetical ancestral mollusk, or HAM. Some workers have

interpreted the Cambrian Burgess Shale taxon Wiwaxia and

other less complete halkieriid-like fossils as molluscan (e.g.,

Conway Morris and Peel 1990), whereas others have argued

Wiwaxia to have annelid worm affinities (e.g., Butterfield

1990). However, the discovery of an articulated halkieriid from

the lower Cambrian and the existence of these and other multishelled

placophorans necessitate the reexamination of longheld

assumptions of molluscan ancestry and monophyly. The

rapidly increasing knowledge of coeloscieritophoran diversity

suggests that we should not rule out the possibility that they

shelter independent ancestors for extant molluscan groups

(Lindberg and Ponder 1996).

Early molecular phylogenies for Mollusca using nuclear

and mtDNA sequences initially had limited success in resolving

a monophyletic molluscan clade or even producing robust

or reasonable groupings within Mollusca (e.g., the

bivalves and gastropods). These problems most likely result

because of the deep, Paleozoic divergence of many of the

molluscan taxa and the variable rates of change in genomes

across taxa. We are now witnessing a new period in molluscan

molecular studies with the addition of new genes, secondary

structures, in situ hybridizations, and more. These

data are currently providing analyses that are converging on

a relatively small subset of polytomies within some molluscan

groups (for a review, see Lydeard and Lindberg 2003).

The major groups of living mollusks are clearly dissimilar

from one another and have long been recognized as distinct

taxa. However, not all were originally recognized as

belonging to Mollusca. For example, the wormlike bodies of

the aplacophorans were perplexing to early biologists and

required study of their internal anatomy to ultimately recognize

their affinities with the other molluscan groups. This

problem becomes especially acute with fossil taxa; the extinct

groups (indicated below with a †) may or may not be mollusks

in our current delimitation of the taxon based on living

representatives. However, it is probable that with some

more inclusive grouping, these fossil taxa share common

ancestors with living molluscan groups.

The converse problem relates to living taxa. For example,

although it is possible to relate living taxa to one another using

both morphologic and molecular characters, there exists

the real possibility that the living taxa do not share a single

most recent common ancestor, but may have had multiple,

independent derivations from distantly related mollusks or

mollusk-like taxa that are now extinct (see below). These and

other alternative hypotheses require that both fossils and living

taxa be studied and incorporated into evolutionary scenarios

and hypotheses of molluscan relationships, especially

when the fossil record provides such a wealth of fossils and

putative relatives.

Possible Mollusks

† Coeloscleritophora—represented worldwide as small,

hollow, calcareous sclerites in the Precambrian and Cambrian.

Insights into these enigmatic fossils have been obtained

from articulated specimens (Conway Morris and Peel 1990,

Bengtson 1992). Nevertheless, their relationship to Mollusca

262 The Relationships of Animals: Lophotrochozoans

remains uncertain, although at least some members of this

possibly polyphyletic group may share common ancestry

with mollusks, annelids, or brachiopods.

† Hyolitha—sometimes treated as a separate extinct

phylum. The hyoliths have bilaterally symmetrical closed

tubes with the aperture closed with an operculum. They first

appear in the Early Cambrian and were extinct by the end of

the Paleozoic (Runnegar 1980).

† Stenothecoida—bivalved Early to Middle Cambrian

fossils in five or six genera that are sometimes regarded as

mollusks (Pojeta and Runnegar 1976, Yochelson 2000).

Waller (1998) considered Stenothecoida to represent the

sister taxon of the Rostroconchia + Bivalvia.

Higher Molluscan Taxa

Polyplacophora (Chitons, Amphineura)

Morphology and Biology

Chitons (fig. 16.7) are flattened and elongate-oval, with eight

overlapping dorsal shell plates or valves, bordered by a thick

girdle that may be covered with spines, scales, or hairs and is

formed from the mantle. The pallial cavity containing multiple

pairs of small gills surrounds the foot, with which the animal

typically clings to hard surfaces. The plates are greatly reduced

or even internal in a few species, these sometimes having an

elongate, somewhat wormlike body. Most are small (0.5–5

cm), but one species reaches more than 30 cm in length.

Chitons possess a heart and an open blood system, a pair

of kidneys that open to the pallial cavity, a simple nervous

system with two pairs of nerve cords, and many special

minute sensory organs (aesthetes) that pass through the shell

valves. Some of these are specialized as light receptors, having

a minute lens and retinalike structure. The mouth is surrounded

by a simple fold, and the head lacks tentacles or eyes.

They feed on encrusting organisms such as sponges and

bryozoans and nonselectively on diatoms and algae that are

scraped from the substrate with their radula, which is hardened

by the incorporation of metallic ions. One group captures

small crustaceans by trapping them under the anterior

part of their body (McLean 1962).

Chitons are generally dioecious, with sperm released by

males into the water. In most chitons, fertilized eggs are shed

singly or in gelatinous strings, and once fertilized in the water

column, these develop into trochophore larvae that soon

elongate and then directly develop into juvenile chitons; there

is no veliger stage. In brooding species the eggs remain in the

pallial cavity of the female, where they are fertilized by sperm

moving through with the respiratory currents. Upon hatching

from the brooded eggs, the offspring may remain in the

pallial cavity until they crawl away as young chitons or exit

the pallial cavity as trochophores for a short pelagic phase

before settling.

Habitat

All chitons are marine, and the group has a worldwide distribution.

Most live in the rocky intertidal zone or shallow

Figures 16.7–16.11. The lesser

molluscan classes. 16.7.

Polyplacophora (chitons;

redrawn from Gray 1850).

16.8. Caudofoveata (or

Chaetodermomorpha; redrawn

from Beesley et al. 1998). 16.9.

Solenogastres (or Neomeniomorpha;

redrawn from Beesley

et al. 1998). 16.10. Monoplacophora

(or Tryblidia; redrawn

from Lemche 1957). 16.11.

Scaphopoda (tusk shells). All

drawings by C. Huffard.

The Mollusca: Relationships and Patterns from Their First Half-Billion Years 263

sublittoral, but some live in deep water to more than 7000

m. A few species are associated with algae and marine plants,

and in the deep sea water-logged wood is a common habitat

for one group.

Diversity and Fossil History

This relatively small group has been estimated to be between

650 and 800 recent species. The group first appears in the

Late Cambrian (Mattheva).

Major Groups

Two groups (Paleoloricata and Neoloricata) are currently

recognized, one of which are extinct. All living chitons are

included in Neoloricata.

State of Knowledge

Our understanding of the species-level diversity of polyplacophorans

has been greatly enhanced by the systematic work

of Kaas and van Belle (1987–1994); Paleozoic taxa have been

recently treated by Hoare (2000). However, given chiton

diversity and abundances along rocky shores, and their importance

in rooting analyses of other putative molluscan

classes, it is surprising that a modern phylogenetic treatment

of the group remains to be done.

Aplacophora (Caudofoveata and Solenogastres

or Chaetodermomorpha and Neomeniomorpha,

Spicule Worms)

Morphology and Biology

These wormlike mollusks (figs. 16.8, 16.9) lack shells but instead

have calcareous scales or spicules in their integument,

and they range in size from 1 mm to 30 cm. Caudofoveates

are burrowers that feed on bottom-dwelling microorganisms

such as formanifera, whereas most soleonogasters feed on

cnidarians. Both groups have a radula and lack true nephridia.

Overall, the aplacophoran body plan is similar to that of

the chitons. Aplacophorans and polyplacophorans differ

from the monoplacophorans by having a dorsal gonad rather

than a posterior gonad. The pericardium is similar in all three

groups, as are many of the other organ systems and positions.

Major differences are found in the type of spicules secreted

by the dorsal mantle epidermis.

The calcareous spicules that cover the bodies of most

aplacophorans give the animals a striking sheen. These spicules

are secreted by the mantle epidermis and are the probable

homologue of the shell of other molluscan groups. Spicule

morphology varies over the body of the aplacophoran, and in

some taxa spicules are modified into scales.

It is the internal anatomy that provides evidence of the

molluscan identity of the aplacophorans. In both groups, the

anterior end of the alimentary system includes a radula and

odontophore. In Chaetodermomorpha, the radula and odontophore

are strongly developed, and the alimentary system

is more differentiated than in Neomeniomorpha. Both groups

have a dorsal gonad that opens into the pericardium, which

contains the heart. From the posterior portion of the pericardium,

there extends a coelomoduct that loops or bends

and ultimately opens into the pallial cavity. In Neomeniomorpha,

the posterior portion of the coelomoducts is modified

for reproductive functions such as sperm storage or

brooding young. The nervous system is ladderlike, with a

well-developed cerebral ganglion. Radular configurations are

quite variable and show a wide range of tooth development

and modifications that include jawlike structures, denticles

with cones, and sweepers. This is second only to the range

of radular variation found in gastropods and is in marked

contrast to the lack of variation found in Monoplacophora,

Polyplacophora, and Scaphopoda.

Development includes trochophores or a test cell larval

stage in which the three tissue types (mesoderm, ectoderm,

endoderm) align and differentiate within an exterior cell layer

constructed of large test cells. Aplacophoran eggs are relatively

large and free-spawned in Chaetodermomorpha and

fertilized internally in Neomeniomorpha; some Neomeniomorpha

members brood their young to various stages of

development. After the formation in the test cell larva of an

apical tuft and prototroch, the posterior development of the

differentiating larva quickly outgrows the exterior test and

develops directly into the juvenile aplacophoran.

Habitat

All are marine and many live in the deep sea (to 6000 m or

more).

Diversity and Fossil History

Around 320 species are known. There are no undoubted

aplacophoran fossils, although some fossil organisms have

been incorrectly attributed to them (e.g., Sutton et al. 2001).

Major Groups

Aplacophora is probably paraphyletic (Haszprunar 2000,

Salvini-Plawen and Steiner 1996), although Scheltema (1996)

regards this taxon as monophyletic and considers it to be

equivalent in rank to the other classes.

Caudofoveata (or Chaetodermomorpha; fig. 16.8). Contains

about one third of the known aplacophoran species, all of

which are footless and vermiform and live in sediments. They

have a circumoral sensory cuticular shield, the midgut separated

into a stomach and glandular digestive diverticulum,

and a pair of ctenidia in the small pallial cavity and are dioecious.

They lack a foot and pedal groove and serial sets of

lateroventral muscle bands.

Solenogastres (or Neomeniomorpha; fig. 16.9). Contains

about two-thirds of the known aplacophoran species, which

typically live in association with cnidarians such as hydroids

and alcyonaceans. They have a narrow foot in a ventral groove

with which they can creep, no oral shield, a sensory supraoral

vestibule, a simple midgut (combined stomach and digestive

gland), and serial sets of lateroventral muscle bands and are

264 The Relationships of Animals: Lophotrochozoans

simultaneous hermaphrodites. They lack ctenidia in the rudimentary

pallial cavity.

State of Knowledge

Recent studies and interpretations of aplacophoran phylogeny

(Haszprunar 2000, Waller 1998) have focused attention

on this small group of mollusks. Primarily because of the

detailed studies (and contrasting interpretations) of Salvini-

Plawen and Scheltema [see references in Haszprunar (2000)

and Waller (1998)], the morphology of aplacophorans are

relatively well known for a numerically and physically smallsized

group of organisms. This knowledge base is even more

remarkable when you consider that this is primarily a deepwater

taxon, but species-level diversity is undoubtedly still

severely understudied in this poorly collected group. Molecular

phylogenetic studies of this taxon are lacking, and its

placement on the molluscan tree remains problematic.

Monoplacophora (Tryblidia, Helcionelloidea,

and Tergomya)

Morphology and Biology

Extant monoplacophorans are small and limpet-like, having

a single, cap-like shell (fig. 16.10). Some organs (kidneys,

heart, gills) are repeated serially, giving rise to the now falsified

hypothesis that they have a close relationship with segmented

organisms such as annelids and arthropods (Wingstrand 1985,

Haszprunar and Schaefer 1997).

In recent and fossil patelliform monoplacophoran shells,

the apex is typically positioned at the anterior end of the shell,

and in some species it actually overhangs the anterior edge

of the shell. Aperture shapes vary from almost circular to pear

shaped. Shell height is also variable and ranges from relatively

flat to tall. The monoplacophoran animal has a poorly defined

head with an elaborate mouth structure on the ventral

surface. The mouth is typically surround by a V-shaped,

thickened anterior lip and postoral tentacles in a variety of

morphologies and configurations. Behind the head lies the

circular foot. In the pallial groove, between the lateral sides

of the foot and the ventral mantle edge, are found five or six

pairs of gills (fewer in minute taxa).

Internally, the monoplacophoran is organized with a

long, looped alimentary system, one to three pairs of gonads,

and multiple paired excretory organs (some of which also

serve as gonoducts). A bilobed ventricle lies on either side

of the rectum and is connected via a long aorta to a complex

plumbing of multiple paired atria. The nervous system is

cordlike and has weakly developed anterior ganglia; paired

muscle bundles surround the visceral mass. Large dorsal

paired cavities are extensions of glands associated with the

esophagus. The monoplacophoran radula is docoglossate,

each row having a central tooth, three pairs of lateral teeth,

and two pairs of marginal teeth. There are no developmental

studies of monoplacophorans.

Recent monoplacophorans form a clade (Wingstrand

1985), and their similarities and differences with the other

extant molluscan groups are easily recognized. There is little

question that some Paleozoic taxa are also members of this

clade. However, the characters that distinguish some Paleozoic

monoplacophorans from the torted gastropods and

vice versa are open to alternative interpretations, and the

relationships of several major groups of early-shelled mollusks

have therefore been the subject of much debate (see

above).

Habitat

Monoplacophorans are found both on soft bottoms and on

hard substrates on the continental shelf and seamounts. Paleozoic

taxa are associated with relatively shallow water faunas

(<100 m).

Diversity and Fossil History

Monoplacophorans are the first undoubted mollusks, being

found from the earliest Cambrian. Although diverse in the

Paleozoic, the first living member of this exclusively marine

taxon was not discovered until 1952 (Lemche 1957). About

25 living species of monoplacophorans have been discovered

worldwide, living at depths between 174 and 6500 m.

Major Groups

Two groups, Helcionelloidea and Tergomya, are often treated

as separate classes or subclasses. Recent monoplacophorans

belong to Tergomya, whereas the youngest known helcionelloideans

are from the earliest Ordovician.

State of Knowledge

Our knowledge of living members of Monoplacophora

comes from the original anatomical description of Neopilina

galathaea by Lemche and Wingstrand (1959). Wingstrand

(1985) added additional observations and interpretations;

Haszprunar and Schaefer (1997a) and Schaefer and Haszprunar

(1997) provide additional anatomy of two Antarctic

species. All of this work has been reviewed by Haszprunar

and Schaefer (1997b).

Paleozoic members of Monoplacophora are still the subject

of much conjecture. Pojeta and Runnegar (1976)

and Peel (1991) consider almost all Cambrian cap-shaped taxa

as well as the coiled Helcionelloida and some, if not all, of

the bellerophontiform taxa to be untorted monoplacophorans,

whereas others, including Knight and Yochelson

(1958), Golikov and Starobogatov (1988), and Parkhaev

(2002), limit the diagnosis of Monoplacophora to capshaped

taxa and consider the remaining Helcionelloida and

bellerophontiform taxa to be torted gastropods. Because

these positions are based on the interpretations of a small

suite of muscle insertion characters and cartoonlike reconstructions

of possible water flow patterns, it is difficult to

test either position.

The Mollusca: Relationships and Patterns from Their First Half-Billion Years 265

Scaphopoda (Tusk Shells)

Morphology and Biology

Scaphopods are benthic, infaunal animals with slender, tubular

shells open at both ends (fig. 16.11). The pallial cavity

is large and surrounds much of the body, and there is a very

simple head and well-developed burrowing foot located at

the ventral (wider) end of the shell. Clublike feeding tentacles

extend from the head, which lacks eyes, and a radula is

present. Paired kidneys are present, but there is no heart (a

reduced pericardium may be present) or gills. Foot morphology

is variable and has been used as a taxonomic character.

Water passing through the pallial cavity enters and exits

through the dorsal aperture.

The scaphopod shell is a calcium carbonate tube with

equal or unequal apertures; the tube may be either inflated

or bowed. The shell microstructure includes prismatic and

crossed-lamellar components; the latter is similar in structure

to elements seen in members of Bivalvia.

Unlike the previously discussed groups, scaphopods have

a U-shaped gut rather than an anterior–posterior configuration

of the mouth and anus. The stomach and digestive gland

are in juxtaposition, and the intestine loops before passing

through the excretory organ and opening into the pallial

cavity. The posterior portion of the digestive gland overlies

the gonad that connects with the pallial cavity via the excretory

organ. The radula consists of a central plate, a single

lateral tooth, and a lateral plate.

The ontogeny of several species has been documented

(Moor 1983, Wanninger and Haszprunar 2001). The trochophore

larva has an apical tuft and prototroch. The foot

rudiment appears early followed by differentiation of the

mantle. The mantle and the protoconch fuse ventrally producing

a characteristic median ventral fusion line on the

embryonic shell. During metamorphosis, the prototroch is

shed and the protoconch stops growing. The adult shell

begins to form, as do the trilobate foot, cephalic captacula,

and the buccal apparatus. Animals are able to feed a few days

after metamorphosis.

Scaphopods have an intriguing set of molluscan characters

that have been allied to several scenarios of molluscan

evolution and relationships. Shell structure and earlier observations

of their development suggest bivalve affinities,

but scaphopods also have a radula. The gross morphology

of the scaphopod gut is U-shaped, like that of gastropods

and cephalopods, rather than linear as in monoplacophorans,

polyplacophorans, and aplacophorans, and recent molecular

studies of shell formation suggest affinities with the gastropods

and cephalopods, as well (Wanninger and Haszprunar 2001).

It has been suggested that scaphopods are descended

from ribeirid rostroconchs (Pojeta and Runnegar 1976),

therefore grouping them with Bivalvia. Although there is

little doubt that scaphopods share some characters with

Bivalvia, the direct derivation of scaphopods from a ribeirid

rostroconch is contradicted by the U-shaped gut present

in scaphopods because rostroconchs are thought to have

had a linear gut based on reconstructions of shell morphology

and musculature.

Habitat

Scaphopods are infaunal organisms and feed on foraminiferans

and other interstitial organisms. They occur from the

intertidal zone to depths in excess of 7000 m and are present

in all the major oceans.

Diversity and Fossil History

There are approximately 600 recent species. Members of the

class first appear in the Early Paleozoic, and the taxon has

maintained a slow but steady rate of increase in morphological

diversification since then.

Major Groups

Two orders, the Dentalida and Gadilida, are recognized.

State of Knowledge

Morphological cladistic analyses of the Scaphopoda have

been performed by Steiner (1992) and Reynolds and Okusu

(1999). A molecular study was conducted by Reynolds and

Peters (1998). However, the relationships within the taxon

are still some way from resolution (Reynolds 1997, 2002).

Several recent morphological analyses (figs. 16.5, 16.6), as

well as unpublished molecular studies (e.g., Steiner and

Dreyer 2002), are resolving Scaphopoda with Cephalopoda

and Gastropoda rather than their more traditional association

with Bivalvia.

Bivalvia (Bivalves, Clams,

Lamellibranchs, Pelecypoda)

Morphology and Biology

Bivalves, including the oysters, mussels, and clams (figs.

16.12–16.14), are the second largest group of mollusks. They

have the shell composed of a pair of laterally compressed

hinged valves, and the pallial cavity surrounds the whole

body (fig. 16.12).

The bivalve shell consists of two valves that are hinged

dorsally, usually with shelly interlocking teeth (the hinge),

and always with a horny ligament that connects the two

valves along their dorsal surfaces and acts to force the valves

apart. The interior of the valves contains scars of the various

muscles attached to it, in particular the (usually two, sometimes

one) adductor muscles that, on contraction, close the

valves. Another scar, the pallial line, represents the line of

attachment of the mantle to the shell, and a posterior embayment

in this line (the pallial sinus) is related to siphonal

length in some bivalves. The shell can be internal and reduced

(or even absent), and the bivalve animal can be wormlike,

such as in “shipworms” (Teredo; fig. 16.14). Bivalve shells are

266 The Relationships of Animals: Lophotrochozoans

constructed of different shell fabrics, including crossed lamellar,

nacreous, and foliated microstructures. Most of the variability

in shell structure sorts along higher taxon divisions.

For example, nacreous structures are present primarily in the

basal members of the group (Protobranchia, Pteriomorpha,

Unionida), whereas crown taxa have primarily crossed lamellar

shells (Heterodonta).

Bivalves typically display bilateral symmetry both in shell

and anatomy, but there are significant departures from this

theme in such taxa as scallops and oysters.

Bivalves lack a buccal apparatus, radula and jaws. Although

the plesiomorphic feeding state for bivalves is probably

deposit feeding using long labial palps, the ctenidia

provide an effective filter-feeding mechanism in most taxa,

with numerous levels or grades of organization. In most bivalves,

the pallial cavity contains a pair of very large gills that

are used to capture food particles suspended in the inhalant

water current. The food is bound in mucus in strings that

are carried by cilia, along food grooves on the edges of the gills,

to the mouth region. Here particles are sorted on the ciliated

labial palps before they enter the mouth. The bivalve stomach

is large and complex with sophisticated ciliary sorting mechanisms

and, usually, a rotating hyaline rod, the crystalline style,

which liberates enzymes into the stomach. Digestion is carried

out in the large paired digestive diverticula.

The visceral mass is primarily situated above the pallial

cavity and continues ventrally into the foot. The intestine is

irregularly looped and opens dorsally into the exhalant area.

Also opening into this region are the paired kidneys and,

when separate from the kidneys, the gonopores of the paired

gonads. The heart typically lies below the center of the valves

and consists of two auricles and a single ventricle that supplies

both anterior and posterior aorta. The nervous system

is made up of three pairs of ganglia. These innervate the oral

apparatus, musculature, mantle, viscera, ctenidia, and siphons.

They receive sensory input from oral lappets, statocysts,

osphradium, various siphonal sensory structures, and

photoreceptors along the mantle margin.

The bivalve foot is modified as a powerful digging tool

in many groups, but in those that live a permanently attached

life (e.g., oysters) it is very reduced. In many bivalve larvae

or juveniles, a special gland, the byssal gland, can produce

organic threads used for temporary attachment. In some

groups, such as mussels, byssal threads permanently anchor

the adults. A few groups of bivalves, such as oysters, are cemented

permanently to the substrate.

The mantle edge in some primitive forms is open around

the entire edge of the shell, but in most bivalves the mantle

is fused to a greater or lesser extent, with openings for the

foot (anterior and ventral) and posteriorly, the exhalant opening

through which the water is expelled from the pallial cavity

and which also carries waste products and gametes. The

inhalant opening, through which water is carried into the

pallial cavity, is also posteriorly located in most bivalves, lying

just below the exhalant opening. In burrowing bivalves,

the mantle edge around the inhalant and exhalant apertures

is extended as separate or fused siphons that can be longer

than the shell length. The mantle edge is also where contact

is made with the external world and is, consequently, where

most sense organs are located. These are usually simple sensory

cells, but in some there are pallial eyes and/or sensory

tentacles.

Bivalves are hermaphrodite or have separate sexes. Eggs

of the protobranchs are large and yolky, whereas those of the

remaining taxa are typically small and not very yolk-rich.

Fertilization is usually external but in brooding species occurs

in the pallial cavity. Cleavage patterns are spiral, and both

polar lobes and unequal cleavage patterns are present throughout

the group. Those embryos developing in the water column

go through both trochophore and veliger (“spat”) larval

stages. Although morphologically similar to the gastropod

veliger stage, phylogenetic analyses (Ponder and Lindberg

1997, Waller 1998) suggest that the veliger stage is homoplastic

rather than homologous. The initial uncalcified shell grows

laterally in two distinct lobes to envelop the body. Larval

bivalves have a byssal gland that may assist with flotation

while planktic but later attaches the juvenile to the substrate.

Many bivalves retain their eggs in the pallial cavity and suck

in sperm with the inhalant water current. In these brooding

bivalves, the larvae develop in special pouches in the gills in

Figures 16.12–16.14. Bivalvia. 16.12.

Cardium (cockle). 16.13. Pectinidae

(scallop). 16.14. Teredo (shipworm). All

redrawn by C. Huffard from Gray (1857).

The Mollusca: Relationships and Patterns from Their First Half-Billion Years 267

some taxa, whereas in others they simply lie in the pallial

cavity. Many brooding bivalves release their young as swimming

veliger larvae, whereas others retain them longer and

release them as juveniles. Freshwater mussels (Unionoidea)

have glochidial larvae that attach to fish as ectoparasites.

Habitat

Most bivalves are marine, but there are also substantial radiations

in brackish and freshwater habitats. They may be

infaunal or epifaunal, and epifaunal taxa may be either sessile

(cemented or byssally attached) or motile (fig. 16.13).

Diversity and Fossil History

The bivalves are an extremely diverse group with about

20,000 living species that range in adult size from 0.5 mm

to giant clams that reach 1.5 m. Although the first occurrences

of Bivalvia are found in Lower Cambrian deposits

(Pojeta 2000), it is not until the Lower Ordovician that

bivalve diversification, both taxonomic and ecological, explodes

in the fossil record. This diversification continues

unabated through the Phanerozoic, with relatively small

losses at the end-Permian and end-Cretaceous extinction

events. Two other extinct Cambrian bivalved groups, Stenothecoida

and Siphonoconcha (Parkhaev 1998), may also

nest within Mollusca, but the absence of bilateral symmetry,

enigmatic hinge structures, and shell composition place

them outside of Bivalvia as currently diagnosed.

Major Groups

Five major groups, usually given the rank of subclass, are

recognized.

Protobranchia are mostly small sized with the hinge typically

composed of many similar, small teeth (taxodont condition)

and include the so-called nut shells (Nuculidae). They

differ from other bivalves in that their large labial palps are used

in deposit feeding and the gills are used only for respiration.

This group is entirely marine, and the interior of the shell is

nacreous in some families. All are shallow burrowers. One

group, Solemyidae, farm symbiotic bacteria in their gills (Kraus

1995) and have a reduced gut. There are about 10, mostly

small-sized families in all. Many are only found in deep water.

Pteriomorphia are an important, entirely marine group that

includes many of the familiar bivalves—scallops (Pectinidae),

oysters (Ostraeidae), pearl oysters (Pteriidae), mussels

(Mytilidae), and arcs (Arcidae)—as well as about 18 other families.

The hinge is taxodont or has a few reduced teeth, or the

teeth are absent. A number of families have lost one of the

adductor muscles (the monomyarian condition), and some

have a nacreous shell interior. Many pteriomorphs are freeliving

epifaunal animals, are byssally attached, or are cemented

and have a reduced foot. Others are shallow burrowers.

Palaeoheterodonta include the broach shells (Trigoniidae)

and the freshwater mussels arranged in two superfamilies—

Unionoidea (Unioniidae, Hyriidae, Margaritiferidae)

and Muteloidea (Mutelidae, Mycetopodidae, and Etheridae).

The shell interior is often nacreous, and the hinge is

composed of a few, often large teeth. All are shallow burrowers.

The freshwater mussels have glochidial larvae that

parasitize fish.

Heterodonta are a large group that includes the majority

of familiar burrowing bivalves—the so-called clams, with

more than 40 families including the very large family

Veneridae, the cockles (Cardiidae), a family that now includes

the giant clams (Tridacnidae), mactrids or trough

shells (Mactridae), and the tellins (Tellinidae). Although

most of the above groups are shallow burrowers, the heterodonts

also include the deep-burrowing soft-shelled clams

(Myiidae), the shipworms (Teredinidae), and rock borers

(Pholadidae). One family (Chamidae) is cemented, and some

members of the very diverse, mostly small-sized Galeommatoidea

are commensals with a wide range of invertebrates.

The shells of heterodonts have a complex hinge composed

of relatively small numbers of different types of teeth, and

the shell is never nacreous. Some members of this group are

found in freshwater (notably Corbiculidae and Sphaeriidae),

and the lucinoids farm symbiotic bacteria in their gills that

provide most of their food requirements.

Anomalodesmata are a rather diverse group includes the

watering pot shells (Clavagellidae) and about a dozen other

small families, some of which are found only in rather deep

water. Members of a few taxa are cemented to the substrate,

but most are shallow burrowers and all are marine. One

group of mostly deep-water families (collectively known as

septibranchs) have the gills modified as pumping septa and

feed on small crustaceans. The shells of some anomalodesmatans

are nacreous, and most have a simple hinge.

State of Knowledge

A Hennigian analysis of bivalve morphology by Waller (1998)

provides an overview of bivalve phylogeny and the relationships

of the bivalves to the other molluscan classes. Waller’s

treatment is also somewhat unique in that it combines both

fossil and living taxa in the analysis. Combined molecular and

morphological studies of bivalve phylogeny have recently

taken a substantial step forward with the high-level analysis

of Giribet and Wheeler (2002). Strictly molecular analyses

of bivalve relationships include Steiner and Muller (1996),

Adamkewicz et al. (1997), and Canapa et al. (1999).

†Rostroconchia

The rostrochonchs look like bivalves but have a single larval

shell that is transformed into a nonhinged, gaping bivalve

shell as the animal grew. They are thought to have evolved

from helcionelloidean monoplacophorans in the Early Cambrian

and underwent an extensive Late Cambrian and Early

Ordovician radiation; they survived until the Permian (Pojeta

and Runnegar 1976). Rostroconchs are thought to share

common ancestry with Bivalvia (Pojeta and Runnegar 1976,

Waller 1998).

268 The Relationships of Animals: Lophotrochozoans

State of Knowledge

The seminal treatment of Rostroconchia is Pojeta and Runnegar

(1976). Waller (1998) provides apomorphies and discussion

of character states for Rostroconchia along with those

for Stenothecidae and Bivalvia.

Gastropoda (Univalves, Limpets, Snails, Slugs)

Gastropods (literally “stomach/foot”; figs. 16.15–16.19) have

figured prominently in paleobiological and biological studies

and have served as study organisms in numerous evolutionary,

biomechanical, ecological, physiological, and behavioral

investigations.

Morphology and Biology

Gastropods are characterized by the possession of a single

(often coiled) shell (figs. 16.15–16.18), although this is lost

in some slug groups (fig. 16.19), and a body that has undergone

torsion (see below) so that the pallial cavity faces forward.

They have a well-developed head that bears eyes and a pair of

cephalic tentacles and a muscular foot used for “creeping” in

most species, while in some it is modified for swimming or

burrowing. The foot typically bears an operculum that seals

the shell opening (aperture) when the head-foot is retracted

into the shell. Although this structure is present in all gastropod

veliger larvae, it is absent in the embryos of some directdeveloping

taxa and in the juveniles and adults of many members

of Heterobranchia. The nervous and circulatory systems

are well developed, with the concentration of nerve ganglia

being a common evolutionary trend.

Externally, gastropods appear to be bilaterally symmetrical;

however, they are one of the most successful clades of

asymmetric organisms known. The ancestral state of this

group is clearly bilateral symmetry (e.g., chitons, cephalopods,

bivalves; see above), but during development their

organ systems can be twisted into figure eights, they can differentially

develop or lose organs on either side of their midline,

or they can generate shells that coil to the right or left.

The best-documented source of gastropod asymmetry is the

developmental process known as torsion. Like other mollusks,

gastropods pass through a trochophore stage and then

form a characteristic stage of development known as the

veliger. During the veliger stage a 180° rotation of the pallial

cavity from posterior to anterior places the anus and renal

openings over the head and twists organ systems that pass

through the snail’s “waist” (the area between the foot and

visceral mass) into a figure eight. This rotation is accomplished

by a combination of differential growth and muscular

contraction. In some taxa the contribution of each process

is about 50:50, but in other taxa the entire rotation is accomplished

by differential growth. Although the results of

torsion are the best-known asymmetries in gastropods, numerous

other asymmetries appear independent of the torsion

process (Lindberg and Ponder 1996). Anopedal flexure

(differential growth that places the mouth and anus in juxtaposition),

which sometimes is considered a feature of torsion,

is widely distributed in Mollusca and is present in the

extinct hyoliths as well as in Scaphopoda and Cephalopoda

(and to a lesser extent in the Bivalvia; Lindberg 1985).

Externally the animal has a well-developed head bearing

a pair of cephalic tentacles and eyes that are primitively situated

near the outer bases of the tentacles. In some taxa, the

eyes are located on short to long eyestalks. The mantle edge

in some taxa is extended anteriorly to form an inhalant si-

Figures 16.15–16.19. Gastropoda.

16.15. Pteropoda (Caenogastropoda).

16.16. Buccinidae (Caenogastropoda).

16.17. Patellogastropoda

(limpet). 16.18. Pulmonate land snail

(Heterobranchia). 16.19. Nudibranchia

(Heterobranchia). All

redrawn by C. Huffard from Gray

(1842; figs. 16.15–16.18) and Gray

(1850; fig. 16.19).

The Mollusca: Relationships and Patterns from Their First Half-Billion Years 269

phon, and this is sometimes associated with an elongation

of the aperture of the shell. The foot is usually rather large

and is typically used for crawling. It can be modified for

burrowing, leaping (as in conchs—Strombidae), swimming,

or clamping (as in limpets; fig. 16.17).

They are extremely diverse in size, body, and shell morphology

and in habits and occupy the widest range of ecological

niches of all mollusks, being the only group to have

invaded the land. Gastropod feeding habits are extremely

varied, although most species make use of a radula in some

aspect of their feeding behavior. Gastropods include grazers,

browsers, suspension feeders, scavengers, detritivores,

and carnivores. Carnivory in some taxa may simply involve

grazing on colonial animals, whereas others engage in hunting

their prey. Some gastropod carnivores drill holes in their

shelled prey, this method of entry having being acquired

independently in several groups (e.g., Muricidae and Naticidae).

Some gastropods feed suctorially and have lost the

radula.

Most aquatic gastropods are benthic and mainly epifaunal,

but some are planktonic—a few, such as the violet snails

(Janthinidae) and some nudibranchs (Glaucus), drift on the

surface of the ocean, where they feed on floating siphonophores,

whereas others (heteropods and Gymnosomata) are

active predators swimming in the plankton (fig. 16.15). Some

snails (e.g., the whelk Syrinx aruanus) reach about 600 mm

in length, but there is also a very large (and poorly known)

fauna of microgastropods that live in marine, freshwater, and

terrestrial environments. It is among these tiny snails (0.5–4

mm) that many of the undescribed species lie.

Most gastropods have separate sexes, but some groups

(mainly the Heterobranchia) are hermaphroditic, although

most hermaphroditic forms do not normally engage in selffertilization.

The basal gastropods release their gametes into

the water column, where they undergo development, but

others use a penis to copulate or exchange spermatophores

and produce eggs surrounded by protective capsules or jelly.

The first gastropod larval stage is typically a trochophore that

transforms into a veliger and then settles and undergoes

metamorphosis to form a juvenile snail. Although many

marine species undergo larval development, there are also

numerous marine taxa that have direct development, this

mode being the norm in freshwater and terrestrial taxa.

Brooding of developing embryos is widely distributed

throughout the gastropods, as are sporadic occurrences of

hermaphrodism in the non-heterobranch taxa. The basal

groups have nonfeeding larvae, whereas veligers of many neritopsines,

caenogastropods, and heterobranchs are planktotrophic.

Egg size is reflected in the initial size of the juvenile

shell or protoconch, and this feature has been useful in distinguishing

feeding and nonfeeding larvae in both recent and

fossil taxa.

Phylogenetic patterns in gastropod evolution often

feature a reduction in the complexity of many characters

(Haszprunar 1988, Ponder and Lindberg 1997). These include

reduction of the number of radular teeth, simplification

(thought to be due to shell coiling) of the renopericardial

system (loss of right auricle and renal organ), reduction of

ctenidia (loss of the right gill), and associated circulatory and

nervous system changes. There is also a reduction of diversity

of shell microstructures, simplification of the buccal

cartilages and muscles, reduced coiling of the hindgut, and

simplification of the stomach. Other characters show an increase

in complexity, such as life-history characters (e.g.,

internal fertilization with penis and spermatophores and

associated reproductive organs). This increase in complexity

is correlated with the ability to produce egg capsules and

the evolution of planktotrophic larvae and direct development.

There is also a phyletic increase in chromosome number,

and greater complexity of sensory structures (e.g., eyes,

osphradium; Haszprunar 1988). In the pulmonates (land

snails; fig. 16.18), the pallial cavity is modified into a pulmonary

cavity or lung, whereas the opisthobranchs (sea slugs)

have secondary gills and elaborate neurosecretory structures.

Habitat

Gastropods occupy all marine habitats ranging from the

deepest ocean basins to the supralittoral, as well as freshwater

habitats and other inland aquatic habitats, including salt

lakes. They are also terrestrial, being found in virtually all

habitats ranging from high mountains, to deserts, to rainforests

and from the tropics to high latitudes.

Diversity and Fossil History

Gastropods are one of the most diverse groups of animals,

in form, habit, and habitat. They are by far the largest group

of mollusks, with more than 62,000 described living species,

and comprise about 80% of living mollusks. Estimates of total

extant species range from 40,000 to more than 100,000 but

may number as high as 150,000, with about 13,000 named

genera for both recent and fossil species (Bieler 1992). They

have a long and rich fossil record from the Early Cambrian

that shows periodic extinctions of subclades followed by

diversification of new groups (Erwin and Signor 1991).

Major Groups

The traditional classification of the gastropods was to divide

it into three subclasses, Prosobranchia, Opisthobranchia, and

Pulmonata. Prosobranchia (= Patellogastropoda + Vetigastropoda

+ Cocculinida + Neritopsina + Caenogastropoda and

some members of Heterobranchia in the classification below)

is paraphyletic, whereas Opisthobranchia + Pulmonata

(Euthyneura) is now known to be but a major clade within

a wider monophyletic group, Heterobranchia. Prosobranchia

were often further divided into Archaeogastropoda, Mesogastropoda,

and Neogastropoda; Archaeogastropoda and

Mesogastropoda are both paraphyletic (Hickman 1988,

Haszprunar 1988, Ponder and Lindberg 1997). There is as

yet no general agreement regarding the ranks applied to the

major groups within the gastropods that have now been

270 The Relationships of Animals: Lophotrochozoans

confirmed from several morphological and molecular studies.

The two main clades (Eogastropoda and Orthogastropoda)

have been used as subclasses, but some authors prefer

to assign subclass rank to the next highest category (Patellogastropoda,

Vetigastropoda, etc.).

Eogastropoda. Patellogastropoda (= Docoglossa) include

the true limpets (Patellidae, Acmaeidae, Lottiidae, Nacellidae,

and Lepetidae). All are marine and limpet-shaped, and many

live in the intertidal zone. This group was previously included

within “Archaeogastropoda.” The shell is foliated in some

taxa, and the operculum is absent in adults. Their radula has

several teeth in each row, some of which are strengthened

by the incorporation of metallic ions such as iron.

Orthogastropoda. Vetigastropoda contain the keyhole

and slit limpets (Fissurellidae), abalones (Haliotiidae), slit

shells (Pleurotomariidae), top shells (trochids), and about 10

other families. All are marine and have coiled to limpetshaped

shells. This group was previously included within

“Archaeogastropoda.” The shell is nacreous in many of these

taxa, and an operculum is usually present. The radula has

many teeth in each row (rhipidoglossate). Many of the hydrothermal

vent taxa are members of this group, including

the neomphalids.

Neritopsina (or Neritimorpha) contain the nerites (Neritidae),

which have marine, freshwater, and terrestrial members,

and a few other small terrestrial and marine families.

They have coiled to limpet-shaped shells, with only one species

(family Titiscaniidae) being a slug. This group was previously

included within “Archaeogastropoda.” The shell is

never nacreous, and an operculum is present in adults. The

radula has many teeth in each row (rhipidoglossate).

Cocculinida contain a group of small white limpets that

occur on waterlogged wood and other organic substrates in

the deep sea. The operculum is absent in adults, and the

radula has many teeth in each row, similar to the vetigastropods

and nerites.

Caenogastropoda are a very large, diverse group containing

about 100, mostly marine families, including littorines

(Littorinidae), cowries (Cypraeidae), creepers (Cerithiidae,

Batellariidae, and Potamididae), worm snails (Vermetidae),

moon snails (Naticidae), frog shells (Ranellidae and Bursidae),

apple snails (Ampullariidae), and a large, almost entirely

marine group of about 20 families that are all carnivores and

belong to Neogastropoda. These include whelks (Buccinidae),

muricids (Muricidae), volutes (Volutidae), harps (Harpidae),

cones (Conidae), and augers (Terebridae). Caenogastropod

shells are typically coiled, a few being limpetlike (e.g., the slipper

limpets, Calyptraeidae), and one family (Vermetidae) has

shells resembling worm tubes. Although most caenogastropods

possess a shell that encloses the animal, it is reduced

in some and has become a small internal remnant in the

sluglike Lamellariidae. Eulimidae are all parasitic on echinoderms;

most are shelled ectoparasites, but some have become

shell-less, wormlike internal parasites. Some groups have

invaded freshwater, the most important being Viviparidae,

Ampullariidae, and Thiaridae (and several closely related

families), and smaller sized snails belong to the diverse families

Hydrobiidae, Bithyniidae, and Pomatiopsidae. There are

a few terrestrial taxa, the cyclophorids being the most significant

family.

Caenogastropods previously consisted of the monophyletic

Neogastropoda and the paraphyletic Mesogastropoda. The

shell is never nacreous, and an operculum is typically present

in adults. Apart from members of Neogastropoda, the radula

usually has only seven teeth in each row (taenioglossate). The

radula of neogastropods has one to five teeth in each row

(stenoglossate); the radula is absent in some.

Heterobranchia are a very large group composed of several

marine and one freshwater group (Valvatidae) that were

previously included in “Mesogastropoda” and two very large

groups previously given subclass status—Opisthobranchia

and Pulmonata (collectively Euthyneura). The more basal

members consist of about a dozen families that are mostly

small sized, mainly rather poorly known operculate groups,

including the sundial shells (Architectonicidae) and a huge

group of small-sized ectoparasites, Pyramidellidae. The opisthobranchs

consist of about 25 families and 4000 species of

bubble shells (Cephalaspidea) and seaslugs (Nudibranchia),

as well as the seahares (Anaspidea). Virtually all opisthobranchs

are marine, with most showing shell reduction or

shell loss and only some of the “primitive” shell-bearing taxa

having an operculum as adults. The pulmonates comprise

the majority of land snails and slugs—a very diverse group

consisting of many families and about 20,000 species. A few

marine pulmonates (including the limpet-shaped Siphonariidae)

comprise groups that mostly inhabit estuaries. A basal

group of mainly estuarine air-breathing slugs (Onchidiidae)

also has terrestrial relatives (Veronicellidae, Rathouisiidae).

Some important groups of freshwater snails are also included

here—the Lymnaeidae, Planorbidae, Physidae, and Ancylidae.

The operculum is absent in all pulmonates except the estuarine

Amphibolidae and the freshwater Glacidorbidae. The

shells of heterobranchs are never nacreous.

State of Knowledge

Although both Haszprunar (1988) and Ponder and Lindberg

(1997) present detailed phylogenetic analysis of Gastropoda,

some of the ordering of the stem-based gastropod groups on

the Tree of Life remains poorly understood, but there is

mounting evidence that Patellogastropoda represents the

sister taxon of all other gastropods. The base of Eogastropoda

remains a polytomy of Cocculinidae, Vetigastropoda, and

Neritopsina in recent analyses. In addition, branching patterns

within relatively well-known groups such as Caenogastropoda,

Vetigastropoda, and Euthyneura can vary markedly

between analyses and data sets. Within Heterobranchia, there

have been recent morphological and molecular analyses of

Nudibranchia by Wagele and Willan (2000) and Wollscheid-

Lengeling et al. (2001), and a recent molecular analysis of

Pulmonata by Wade et al. (2001).

The Mollusca: Relationships and Patterns from Their First Half-Billion Years 271

Cephalopoda (Octopuses, Squids, Cuttlefish,

Chambered Nautilus)

Morphology and Biology

Cephalopods (literally “head-foot”) are dorsiventrally elongated

(figs. 16.20, 16.21), have well-developed sense organs

and large brains, and are thought to be the most intelligent

of all invertebrates. Nearly all are predatory, and most very

active swimmers. A few taxa are benthic, drifters or medusalike,

and some are detritus feeders. All are active carnivores

in marine benthic and pelagic habitats from nearshore to

abyssal depths. Giant squid (Architeuthis) are the largest invertebrates,

and the cephalopods include the largest living

as well as largest extinct mollusks: ammonite shells extend

to more than 2 m across, and body sizes of living squid extend

up to 8 m, with tentacles exceeding 21 m in length. The

smallest cephalopods are around 2 cm in length.

Cephalopods are the most complex and motile of the

nonvertebrate metazoans and show numerous modifications

of the general molluscan body plan. The chambered nautilus

has an external shell, but all other living cephalopods have

either reduced and internalized the shell or have lost it completely.

The calcareous shell of Sepia or cuttlefish (the cuttlebone)

is internal, as is that of the ram’s horn squid (Spirula),

but other squid have the shell reduced to a horny pen, and

octopuses lack a shell. The shells of cephalopods (other than

the reduced gladius or pen in squids) have gas-filled chambers

that assist with buoyancy.

Cephalopods have an amazing ability to rapidly change

color (using numerous chromatophores in the skin), body

shape, and texture, all of which is under nervous control.

Their highly developed, efficient circulatory system differs

from that of other mollusks in being closed and including a

pair of accessory hearts (except in Nautilus). Most cephalopods

can swim using jet propulsion, the pulses generated by

the muscular walls of the pallial cavity. Some also use undulating

movements of paired fins at the distal end of the mantle

for swimming. Many can expel a cloud of ink to create a

“smoke screen” to assist escape. Tentacles (cephalic in origin)

surround the mouth on the head and capture prey. They

often bear suckers, sometimes hooks, and a pair of retractile

tentacles (arms) is found in some groups. They have powerful,

modified jaws (beaks) and a small radula. The gut is

dominated by muscle and enzymes and uses extracellular

digestion. The large salivary glands in some squids and octopuses

can produce highly toxic venoms, and there is a large

digestive gland. The muscular stomach mixes the enzymes

and food and passes the semidigested contents to a large

caecum, where ciliated leaflets sort the particles.

The nervous system is highly advanced, with three major

ganglia concentrated to form a large, efficient brain that

is further enhanced by the formation of lobes. Coleoid

cephalopods also have two large stellate ganglia on the

mantle that control both respiratory and locomotory functions

of the mantle. Experiments on cephalopods have been

shown that they can learn and have good memories and

excellent powers of discrimination (Hanlon and Messenger

1996). Their eyes are by far the most advanced in the

invertebrates, are strongly convergent on vertebrate eyes,

and are capable of resolving brightness, shape, size, and

orientation. Additional sensory structures include statocysts

and olfactory organs.

Cephalopods have a single gonad and separate sexes, with

males transferring spermatophores to females after typically

complex courtship. The spermatophore is transferred by the

male using a penis (some squid, vampire squids, and cirrate

octopuses) or (in nearly all others) a modified arm (hectocotylus).

Nautilus uses four modified arms. Some taxa are

highly sexually dimorphic. Fertilization is internal, with egg

capsules being laid, and development is direct. Eggs are large

and yolk-rich. There is no larval stage, just direct development

into juveniles, although, as in some benthic taxa, these

may have a pelagic phase. Both the eggs and young may be

brooded, benthic, or pelagic. The shell of the paper argonaut

(Argonauta) is the egg case, not a true shell.

Cephalopods are thought to have evolved from monoplacophoran-

like ancestors (Pojeta and Runnegar 1976).

Septa formed at the apex as the animal grew and withdrew

into a newly formed body chamber. The old chambers are

gas filled and provide buoyancy for the organism. The foot

was modified into a funnel that provided jet propulsion for

movement.

Habitat

Cephalopods are found worldwide, all are marine, and only

a few can tolerate brackish water. All are found in benthic

and pelagic habitats from nearshore to abyssal depths.

Figures 16.20 and 16.21. Cephalopoda. 16.20. Decabrachia

(squid). 16.21. Octobrachia (octopus). All drawn by C. Huffard.

272 The Relationships of Animals: Lophotrochozoans

Diversity and Fossil History

Cephalopods were once one of the dominant marine animals,

but there are only about 700 living species. More than 20,000

species are known as fossils.

Cephalopods are much more variable in their diversity

through time than are other molluscan groups. They have

experienced numerous extinctions (e.g., terminal Permian,

Triassic, Cretaceous events) but typically showed rapid replacement

(and subsequent radiation) by the survivors.

Major Groups

Three major clades (usually treated as subclasses) are recognized:

Nautiloidea, Coleoidea, and Ammonoidea.

Nautiloidea include the pearly or chambered nautilus and

its many fossil relatives. They first appeared in the Late Cambrian

and underwent a rapid diversification in the Ordovician.

All have a spiral nacreous shell with interconnected

internal chambers. The head is covered with a hood and has

numerous short, suckerless tentacles; there are two pairs of

gills and no ink sac.

Coleoidea have 8–10 suckered or hooked tentacles and

a single pair of gills, and an ink sac is often present. There

are two main groups: Octobrachia and Decabrachia. Octobrachia

(= Octopodiformes; fig. 16.20) includes octopuses,

paper argonauts, the pelagic cirrate octopods (Octopoda),

and vampire squid (Vampyromorpha). These all have four

pairs of tentacles and no internal shell. Decabrachia

(fig. 16.21) contains the ram’s horn squid (Spirulida), the

cuttlefish and dumpling squid (Sepioidea), and the squid

(Teuthoidea). These all have four pairs of nonretractable arms

and one pair of retractable arms (tentacles), and most have

an internal shell (reduced to a chitinous pen in squids). The

extinct Belemnoidea also belongs to this group.

Ammonoidea are a large, diverse clade of extinct shelled

cephalopods that appeared in the Devonian and died out at

the end of the Mesozoic. Impressions of animals suggest that

they had 8–10 tentacles.

State of Knowledge

The last few years have witnessed a substantial increase in

morphological, molecular, and combined analyses of cephalopod

groups. Early morphological analyses include Young

and Vecchione (1996; coleoid cephalopods) and Anderson

(1996; loliginid squids). Concurrent molecular analyses include

Bonnaud et al. (1996; also coleoid cephalopods) and

Boucher-Rodoni and Bonnaud (1996) and Bonnaud et al.

(1997), who examined higher level cephalopod relationships.

More recently, Vecchione et al. (2000) investigated the

relationships of neocoleoid cephalopods using molecular

characters, and Anderson (2000a, 2000b) first used mtDNA

sequences and then combined data sets to further examine

relationships among the loliginid squids. Molecular and

morphological data sets have also been compared in the

analysis of Octopoda by Carlini et al. (2001). Phylogenetic

analyses have recently extended back into deep time with

morphological analyses of Neoammonoidea (Engeser and

Keupp 2002) and the hamitid ammonites (Monks 2002).

The Future: Significant Problems Remaining,

New Developments, and Targets

As discussed above, there remains a lack of resolution of the

sister taxon to Mollusca. Convincing resolution of this problem

will require new molecular data, acquisition of additional

detailed morphological (including ultrastructure and immunocytochemistry)

data for adults and larvae, and developmental

information, for basal molluscan taxa and putative

outgroups.

There is an urgent need for more sequence data in all

groups, especially from a larger set of genes, both coding and

noncoding. In addition, data sets using secondary structure

(Lydeard et al. 2000, 2002) and mtDNA gene order (Boore

and Brown 1994, Ueshima and Nishizaki 1994) have already

proved to have great potential utility. There is a need to resolve

not only the deep branches (the relationships of the

“classes”) but also the relationships within the major monophyletic

groups, virtually all of which have Paleozoic roots.

For example, within the gastropods, the placement of neritopsines

and various groups of limpets on the tree is still problematic,

in part because of long-branch attraction (Colgan

et al. 2000). The development of methodologies to overcome

long-branch problems would greatly benefit such studies.

Many long branches cannot be easily resolved (e.g., by

adding additional taxa) because of the extinction of major

clades. Incorporation of these extinct taxa in phylogenetic

reconstructions may be difficult with mollusks because most

of the characters used (anatomical, cytological ultrastructural,

molecular) are not preserved. However, shell characters have,

when properly used, been shown to be as useful as other

characters at various levels of phylogenetic reconstruction

(Wagner 1996, Schander and Sundberg 2001), especially if

preservation is adequate to enable the incorporation of the

fine structure of larval shells or shell microstructure. Such

findings give more hope that the relationships of Paleozoic

and Mesozoic taxa will ultimately be successfully resolved,

and as argued above, there exists the real possibility that the

recognized groupings of living taxa do not share a single

common ancestor but may have had multiple, independent

derivations from distantly related mollusks or mollusk-like

taxa that are now extinct.

Phylogenetic resolution within non-gastropod clades is

also fragmentary, poorly resolved, or lacking. There is a continuing

need of better, parallel anatomical data for many

groups and more comprehensive, phylogenetically based,

comparative studies of organ systems (Ponder and Lindberg

1996), ideally incorporating histological studies.

Several ultrastructural data sets have contributed considerably

to our understanding of molluscan, and especially

gastropod, phylogeny. In particular, data on the osphradium

The Mollusca: Relationships and Patterns from Their First Half-Billion Years 273

(Haszprunar 1985a) and sperm (Healy 1998, Buckland-

Nicks 1995) have made major contributions, whereas smaller

data sets such those on cephalic tentacles in gastropods

(e.g., Kьnz and Haszprunar 2001) and details of the central

nervous system (Huber 1993) have added important

markers. Additional data on other systems, such as the work

of Lundin and Schander (2001a, 2001b, 2001c) on cilial

ultrastructure, is needed to expand coverage and provide

additional characters. The recent compilation by Harrison

and Kohn (1994, 1997) and their colleagues provides a

comprehensive overview of the state of our knowledge in

molluscan ultrastructure.

The use of developmental data has been extremely important

in delineating spiralian taxa but has only infrequently

been used in studies on molluscan phylogeny. Only three of

the 117 characters used in Ponder and Lindberg’s (1997) data

set were developmental, mainly because of the lack of data

for many of the critical taxa. Freeman and Lundelius (1992),

van den Biggelaar and Haszprunar (1996), and Guralnick and

Lindberg (2001) have shown that cleavage patterns and cell

lineages can be successfully employed in reconstructing gastropod

phylogeny. Studies on organogenesis have provided

many valuable insights but are currently unfashionable, although

the use of transmission electron micrography has

been shown to be a valuable tool to provide much improved

interpretation (e.g., Page 1998). Other imaging techniques

such as confocal microscopy have been used to examine the

development of musculature and other organ systems in

chitons (Wanninger and Haszprunar 2002a), scaphopods

(Ruthensteiner et al. 2001, Wanninger and Haszprunar

2002b), and gastropods (Wanninger et al. 1999), resulting

in the resolution of several long-standing controversies. And

although we may not agree with the phyletic placement of

the spiculate animals described by Sutton et al. (2001), the

imaging techniques used to resurrect these creatures from

solid rock will likely provide researchers with a wealth of new,

detailed morphological data from deep time.

Although the literature has many detailed descriptions

of larval development for higher gastropods and bivalves,

there are relatively few for basal taxa. Comparative studies

on trochophore and veliger larvae to address phylogenetic

questions within mollusks are a potentially valuable field of

study. For example, it has been suggested that planktotrophy

may have arisen as many as three times within gastropods

based on supposed larval differences (e.g., Ponder 1991,

Ponder and Lindberg 1997), but no study has yet made a

detailed comparison of the larvae from all three feeding clades

(Neritopsina, Caenogastropoda, and Heterobranchia), and

the most parsimonious scenario remains a single origination

(Lindberg and Guralnick 2003).

Some of the issues identified above result from the unequal

coverage and treatment of molluscan groups. For example,

the number of papers with “Gastropoda” appearing

as a key word in the BIOSIS literature database (available at

http://www.biosis.org/) is in excess of 15,000 papers over the

last 8 years, whereas “Monoplacophora” papers number only

30 (fig. 16.22: solid bars). However, these numbers can be

misleading relative to the biodiversity of these groups, and a

more accurate metric might be the ratio of “species” to papers

(fig. 16.22: open bars). Using this ratio, the Monoplacophora,

Bivalvia, and Cephalopoda are actually pretty well represented

by research publications (the latter two taxa most

likely because of their commercial importance, the former

because of its status as a supposed “living fossil”). Although

the relatively understudied status of Aplacophora, Polyplacophora,

and Scaphopoda is not surprising (see also Lindberg

1985), this status for Gastropoda may come as a surprise to

many given the seeming overabundance of gastropod work-

Figure 16.22. Research effort on major

living molluscan taxa. Data from BIOSIS

key word searches of papers published

from 1995 through 2002. Solid bars,

number of taxon papers; open bars,

number of “species” estimated in each

taxon, divided by the number of taxon

papers.

Taxa

APLAC POLY MONO BIV SCAP CEPH GAST

No. of papers

100

101

102

103

104

105

106

Taxa:paper ratio

100

101

102

103

104

105

106

0.67 0.73 0.17

274 The Relationships of Animals: Lophotrochozoans

ers and publications relative to other molluscan groups. However,

the sheer diversity of this group simply overwhelms

even this relatively large number of workers.

Conclusions

Although great progress has been made over the last 15 years

to resolve molluscan relationships, their relationships to

other spiralian taxa, and thus their precise placement on the

Tree of Life, remain unresolved. Within mollusks, different

data sets are used in phylogenetic studies and in developing

evolutionary scenarios. These include fossils (shell morphology),

anatomy and histology, larval characters, ultrastructure,

and molecular data. More recently, there have been some

attempts to combine some or all of these kinds of data. However,

robust hypotheses of molluscan origins and finer level

relationships still appear to be some way off. This is unfortunate

because the lack of such hypotheses (and the resultant

stable classifications) may contribute to the lack of a

modern (post-1960) treatment of Mollusca in many textbooks

(e.g., Brusca and Brusca 2002) and to the continued

use of paraphyletic taxa, falsified evolutionary scenarios, and

just-so stories in teaching and the popular literature.

In a more positive light, phylogenetic studies of molluscan

groups have produced many new insights into molluscan

evolution, especially in Gastropoda, and many of these

patterns are also present in other molluscan groups, and at

the level of Mollusca as well. These include pronounced

asymmetries in diversity, morphology, and ecology; evolutionary

patterns in respiration and ventilation; phyletic

changes in early developmental timing; and stunning examples

of morphological and biological convergence. Evaluation

of these and other character distributions, as well as

testing of alternative hypotheses of molluscan evolution,

requires a rigorous phylogenetic analysis of the data and continuing

evaluation of the alternative theories and interpretations.

New approaches such as gene expression and mtDNA

gene order are beginning to be employed to resolve phylogenetic

questions, but there is also a great need for additional

data in more traditional areas on critical taxa (e.g., detailed

anatomy, histology, ultrastructure, developmental data, and

standard sequencing). With their diversity, abundance, and

excellent fossil record, mollusks are an excellent group for

exploring a wide range of evolutionary hypotheses. Wellresolved

phylogenies will undoubtedly reduce the variance

in all investigations and markedly enhance the already rich

literature on the genetics, diversity, and ecology of mollusks

that have provided important insights into evolutionary biology,

biogeography, and ecology in general.

Acknowledgments

We thank J. Cracraft and M. Donoghue for the opportunity to

participate in the Assembling the Tree of Life symposium, and

P. D. Johnson and C. Lydeard for sharing their knowledge of

freshwater molluscan faunas with us. The manuscript was

improved by the comments of an anonymous reviewer and the

artistic talents of C. Huffard.

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VII

The Relationships of Animals: Ecdysozoans

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