15 Toward a Tree of Life for Annelida

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Mark E. Siddall

Elizabeth Borda

Gregory W. Rouse

237

The basic characteristics of Annelida, the quintessential

“worms,” are immediately recognizable to most people, if only

from having seen countless earthworms creeping over grass

or braving the streets after a hard summer rain. The most

recognizable feature of annelids, besides their shape and

propensity for exuding mucus when disturbed, is the segmented

nature of their bodies. This segmentation, or “somatic

metamerism,” has been central in the history of ideas about

their relationships, although it is thought now to have been

somewhat misleading. From the iceworms living deep in the

Gulf of Mexico to the Pompeii worm that can withstand water

temperatures that approach boiling, it is clear that annelids

are a remarkably diverse group with a range of morphologies,

life history strategies, and habitat preferences that rivals

any other group of organisms considered in this volume.

Although clearly the oligochaetes (which includes the earthworms)

would probably be the most readily recognized as

belonging to this group, there are also the much more numerous,

principally marine, bristleworms (or polychaetes) and, of

course, the much-maligned leeches (fig. 15.1). Additional, less

known groups belong to the phylum Annelida, and whether

or not others have evolved from annelid ancestors remains a

matter of debate and intense scientific scrutiny.

The importance of annelids to ecology received a considerable

boost in the 1800s with Charles Darwin’s (1881) detailed

demonstration that earthworms are responsible for recycling

and aerating soils. Since that time, and particularly in the last

century, annelid species have been central in assessments of

water quality both in freshwater and in marine ecosystems as

indicators of oxygen content, salinity, organic chemical pollutants,

and heavy metal concentrations (Lauristen et al. 1985,

Uzunov et al. 1988, Metcalfe et al. 1988, Verdonschot 1989,

McNicol et al. 1997). The ubiquitous use of worms as bait by

sport fishermen is testament to the direct role worms play in

global food webs, where they may constitute more than onethird

of the benthic animal diversity associated with coral reefs

or intertidal shore life (Grassle 1973).

But, too, there is a darker ecological side to annelids as it

relates to their parasitological role. Although, generally speaking,

leeches are painless thieves of scant quantities of blood

from unsuspecting hosts, a few transmit deadly blood flagellates

to their victims. Small tubificid oligochaetes serve as the

intermediate hosts for myxosporeans that cause “whirling

disease” in salmon by infecting the brain and other neurological

tissues of the fish (Kent et al. 2001). Even a few of

the marine polychaetes have been found to wreak havoc on

important mollusk species by boring into their shells and thus

threatening millions of dollars of fishery resources and aquaculture

operations (Fitzhugh and Rouse 1999, Kuris and

Culver 1999, Lafferty and Kuris 1996).

As with most of the major branches on the eukaryotic

tree, our understanding of the anatomical and ecological

complexities of annelids would be greatly enhanced with a

solid accounting of the evolutionary history of the group. For

example, if we knew where leeches came from (or, specifically,

with which group they share a recent ancestry), we

238 The Relationships of Animals: Lophotrochozoans

might be afforded important clues regarding the origins of

the very powerful salivary compounds they harbor that prevent

blood from clotting, which in turn might open new

avenues for research into treating those prone to strokes or

heart disease. Thankfully, there has been good progress in

this direction in the last decade. We now have a more complete

picture of what annelids are related to, what groups of

worms should rightly be included in the phylum, and in

certain instances a very good idea of how portions of the

annelidan tree have branched and diversified. However, important

gaps remain in our knowledge in each of these three

contexts. It is our hope that this chapter will stimulate greater

interest in solving those concerns once and for all.

The Sister Search

The enormous subkingdom of life “Vermes” created by Linnaeus

was not taken seriously for very long—not even, it

seems, by Linnaeus himself. Granted, there was the superficial

similarity among wormy animals in that they lacked

prominent appendages and were longer than they were wide,

but there was little else (save convenience) to suggest this

potpourri of animal life should be held together. Soon

Linnaeus began the deconstruction of Vermes, first by removing

snakes to a more sensible location with other vertebrates.

Similarly, near the beginning of his career, Lamarck

(1802) recognized the segmented nature (fig. 15.2) of a large

collection of the remaining worms, creating the taxon

Annйlides (= Annelida) for them but leaving the remainder

in Vermes.

Almost immediately, differences in opinion arose regarding

the closest relatives to annelids. Lamarck (1809) clearly

had them grouped with mollusks in a derivation separate

from the insects and crustaceans. However, Lamarck’s chief

detractor, Georges Cuvier, placed annelid worms with the

arthropods together as one of the major “embranchments”

of life, creating what we would today regard as the superphylum

Articulata (Cuvier 1812). The principal rational for

this amalgamation of worms possessing a hydrostatic skeleton

with crustaceans and insects possessing an exoskeleton

was the recognition that each exhibits a longitudinal repetition

of portions of the body in which the segments are separated

by walls or septa. The influential Haeckel (1866) agreed

that this axial mesodermal somatic metamerism justified the

Figure 15.1. Three among many of the principal groups of

annelids are polychaetes, oligochaetes, and leeches, represented

here by a syllid polychaete (top), a glossoscolescid earthworm

(middle), and a glossiphoniid leech (bottom). Photos by

G. Rouse (top) and M. Siddall.

Figure 15.2. An obvious feature of annelids, yet one that

historically has led to come confusion regarding relationships, is

their segmentation. The name “Annelida” is derived from the

Latin word for “ring.” Each body ring, or somite, is separated

from the next by a septum, and each has a series of structures

that repeats in successive somites through the body. Photo by

G. Rouse; drawing modified from Rouse and Pleijel (2001).

Toward a Tree of Life for Annelida 239

grouping and drew Articulata as one of the largest limbs

emerging from his stylized tree of life (depicted in the introduction,

fig. I.2). After the Darwinian revolution, this affiliation

of annelids and arthropods carried more weight in that

there was an easy suggestion of a “transitional form” between

annelids and arthropods embodied by the limbed onycophoran

velvet worms (e.g., Snodgrass 1938, Meglitsch and

Schram 1991). A few systematists continued to wonder

whether or not Lamarck was right in grouping annelids with

mollusks (e.g., Pelseneer 1899, Naef 1913), but this hypothesis

did not receive serious consideration until the advent of

molecular phylogenetics in the 1980s.

The availability of universal primers for PCR (polymerase

chain reaction) amplification and sequencing of the ribosomal

DNA (rDNA) encoding the small subunit (SSU, 18S) of

ribosomal RNA (rRNA) provided a means for testing many

notions about the evolutionary history of groups of organisms

(Medlin et al. 1988). One of the first groupings to come

into doubt in light of these new data was Cuvier’s Articulata.

Contrary to the broadly held and widely taught belief in the

primacy of somatic metamerism, 18S rDNA suggested a monophyletic

group comprising onychophorans and arthropods,

quite separate from another that included mollusks and annelids

(Field et al. 1988, Ghiselin 1988). It was quickly recognized

that, although this would require independent

evolution of metamerism, the latter group was characterized

by the presence of pelagic trochophore larvae. Those molecular

results were quickly corroborated by additional DNA data

(Lake 1990) and by an analysis of morphological characters

(Eernisse et al. 1992), but they then came into doubt again

in the face of contradictory analyses both of molecular and

morphological data sets (Wheeler et al. 1993, Rouse and

Fauchald 1995). Eventually the weight of evidence continued

to mount against Cuvier’s Articulata. Since 1995, reanalyses

of rRNA genes and morphological data, whether separately

(Conway Morris and Peel 1995, Ax 1996, Halanych et al.

1995, Winnepenninckx et al. 1995, Aguinaldo et al. 1997)

or in combination (Zrzavэ et al. 1998, Peterson and Eernisse

2001), or of mitochondrial gene sequences (Garcia-Machado

et al. 1999) and even mitochondrial gene order (Boore and

Brown 2000), all indicate that Annelida has a more recent

common ancestry with Mollusca and other groups in

Lophotrochozoa than with Arthropoda and what are now

known as the molting Ecdysozoa.

What Is a Worm and What Is It Not?

Commensurate with the difficulties in determining the differences

between the Articulata hypothesis and the Trochozoa

hypothesis have been those associated with the specific composition

of Annelida itself. Many early phylogenetic analyses

of the problem suffered from presuming that various

groups were monophyletic, such as by including a single

taxon “Annelida” or only a few representatives of the group

(e.g., Eernisse et al. 1992, Wheeler et al. 1993). As such,

higher level determinations that tested whether or not annelids

and arthropods had a recent common ancestry did not

necessarily settle the question of just what is an annelid.

Polychaetes and oligochaetes have hairlike chaetae (or setae)

projecting from each of their body somites (indeed, their

names effectively mean very hairy and a little hairy, respectively),

but then so do other animals, such as brachiopods,

echiurans, and beard-worms (pogonophorans). Besides,

leeches have no hairs at all, and no one doubted that leeches

are related to oligochaetes. These latter two groups comprise

the larger Clitellata by virtue of each having the saddlelike

clitellum about one-third of the way down from the head.

On close examination in a modern phylogenetic context,

Rouse and Fauchald (1995) noted that, with the possible

exception of the presence of a “nuchal organ,” there was no

reason to suppose even Polychaeta to be monophyletic, much

less Annelida, if various groups such as pogonophorans were

excluded.

The pogonophorans (which includes deep-sea hydrothermal

vent Vestimentifera) are marine tube-forming worms

that have an occluded gut and do not exhibit metamerism

in the same way that annelids do. The varied and complex

taxonomy of the group represents one of the more fascinating

tales in animal systematics (see Rouse 2001). The fact that

they tend to be found in deep-sea sediments resulted in the

first member of this group, Siboglinum weberi, not being described

until 1914. The anatomy of the worms was variously

interpreted during the 20th century such that some were

described in a way that was upside down and the larvae were

back to front. Complete specimens of the worms were not

even found until the 1960s. There are now more than 100

nominal species described, most from abyssal regions. Some,

such as Riftia, are large and spectacular members of hydrothermal-

vent communities (Jones 1981), whereas others are

smaller and found in association with reducing sediments,

methane seeps, rotting whale carcasses, or with sunken terrestrial-

plant debris. The nutritional requirements for these

worms are met through their symbiotic relationship with

chemoautotrophic bacteria that occupy cells in the expanded

gut wall (Southward 1993). Riftia pachyptila has the fastest

growth rate of a marine invertebrate: it can colonize a new

hydrothermal vent site, grow to sexual maturity, and have

tubes of 1.5 m in length, all in less than two years (Lutz et al.

1994). This rapid growth would appear to be essential because

their habitat is ephemeral and lasts for only a few years

or decades. In contrast, Lamellibrachia that live in cold seeps

on the Louisiana slope (Gulf of Mexico) grow very slowly,

reaching more than 2 m in tube length but taking more than

100 years to do so (Fisher et al. 1997).

Shortly after their discovery, there was some suggestion

that pogonophorans may be related to the polychaetes

(Uschakov 1933, Hartman 1954), although others considered

them to be more similar to the hemichordate acorn

worms. The spiralian nature of pogonophorans was eventually

conceded, but most invertebrate systematists continued

to hold them to be in a separate phylum (e.g., Nшrrevang

240 The Relationships of Animals: Lophotrochozoans

1970, Ivanov 1988). Rouse and Fauchald’s (1995) work indicated

that morphological data were unable to separate

pogonophorans and vestimentiferans from the polychaetes

and predicted that these aberrant worms would eventually

group with the sabellid polychaetes (which also form protective

tubes). Shortly thereafter, this hypothesis was corroborated

in the context of morphological assessments of

polychaetes (Bartolomaeus 1995, Rouse and Fauchald 1997),

and these odd worms are now included among polychaetes

in the family Siboglinidae (fig. 15.3).

Initial attempts to confirm these results using elongation

factor gene sequences (McHugh 1997) offered some corroboration

of the polychaete ancestry for these extraordinary

deep-sea worms but also suffered from the use of too few taxa

or too small a portion of the gene (Siddall et al. 1998). Eventually,

the combined use of histone gene sequences and

ribosomal gene sequences (Brown et al. 1999) lent strong

support to the morphological results previously obtained

(fig. 15.3). Even mitochondrial gene order corroborates the

annelidan origins for the Siboglinidae (Boore and Brown

2000). Each of those analyses, in addition to demonstrating

that Polychaeta logically had to include the pogonophorans,

also indicated that the clitellate annelids [Oligochaeta and

Hirudinida (leeches)] arose from within the polychaetes, and

that possibly so too did the spoon-worm echiurans.

Regarding the latter, several analyses place Echiura either

within Annelida (McHugh 1997, Brown et al. 1999), sister to

Annelida (Brown et al. 1999), or perhaps closer to Mollusca

(Siddall et al. 1998). The body of echiurans is unsegmented

with an extrusible proboscis anteriorly and with hooks posteriorly.

Their trochophore larval stages are similar to certain

polychaetes. Although common in intertidal zones around the

world, there are few more than a hundred species described

(more from lack of interest than lack of diversity). The Californian

“innkeeper worm,” Urechis caupo, lives in a U-shaped

burrow providing a safe home to several species of crabs, polychaetes,

and even small fish (Arp et al. 1992).

The position of Echiura remains problematic, and molecular

data have also recently necessitated the removal of

myzostomids (a strange group of ectosymbiotic worms once

thought to be annelids) from Annelida in light of their closer

relationship to rotifers and acanthocephalans (Zrzavэ et al.

2001). Meanwhile, there is vanishing support for the notion

that Polychaeta constitute a natural group; rather, they are

expected to be found to be synonymous with Annelida as a

whole (Rouse and Fauchald 1998).

Clitellata: From the Leaves to the Trunk

Although the preceding efforts progressed in terms of delineating

the limits of Annelida from the bottom of the spiralian

tree upward, several researchers have been engaged in ascertaining

the relative relatedness of subsets of annelids such as

the leeches, the tubificid oligochaetes, and other groups, all

Figure 15.3. Morphological data (top, slightly modified from

Rouse and Fauchald, 1997, their fig. 58) and molecular data

(bottom, tree redrawn from Brown et al. 1999). Both provide

support for the hypothesis that pogonophorans and vestimentiferans

(Siboglinidae) evolved from within Polychaeta. The latter

result suggests that oligochaetes and leeches (Clitellata) also are

derived from polychaetes. If correct, Polychaeta would be

synonymous with Annelida. The position of echiurans remains

unclear.

Sipuncula

Echiura

Clitellata

Cossuridae

Opheliidae

Scalibregmatidae

Questidae

Orbiniidae

Paraonidae

Oweniidae

Frenulata

Vestimentifera

Sabellariidae

Sabellidae

Serpulidae

Chaetopteridae

Longosomatidae

Magelonidae

Poecilochaetidae

Apistobranchidae

Spionidae

Trochochaetidae

Capitellidae

Arenicolidae

Maldanidae

Cirratulidae

Acrocirridae

Flabelligeridae

Terebellidae

Trichobranchidae

Pectinariidae

Alvinellidae

Ampharetidae

Amphinomidae

Euphrosinidae

Onuphidae

Eunicidae

Dorvilleidae

Lumbrineridae

Pholoidae

Sigalionidae

Eulepethidae

Polynoidae

Acoetidae

Aphroditidae

Chrysopetalidae

Syllidae

Pilargidae

Sphaerodoridae

Hesionidae

Nereididae

Nephtyidae

Lacydoniidae

Phyllodocidae

Pisionidae

Paralacydoniidae

Glyceridae

Goniadidae

Nematoda

Platyhelminthes

Echiura

Sabellidae

Spionidae

Serpulidae

Opheliidae

Maldanidae

Glyceridae

Sipuncula

Amphinomidae

Fauveliopsidae

Sabellariidae

Sternaspidae

Cirratulidae1

Cirratulidae2

Nephtyidae

Oweniidae

Chaetopteridae

Nereididae

Polynoidae

Sigalionidae

Eunicidae

Lumbrinereidae

Clitellata

Siboglinidae

Terbellidae1

Terebellidae3

Terebellidae2

Molecular Morphology

Vent worms

Pompeii worms

Christmas Tree worm

Bamboo worms

Medusa worms

Feather Dusters

Palolo worms

Leeches and Earthworms

Icecream Cone worms

Bloodworms

Scale worms

Palp worms

Clam worms

Vent Worms

Christmas Tree worm

Bamboo worms

Medusa worms

Feather Dusters

Palolo worms

Leeches and Earthworms

Bloodworms

Scale worms

Palp worms

Clam worms

Toward a Tree of Life for Annelida 241

with the expressed intention of eventually combining their

data in a larger analysis of clitellate annelids. This top-down

approach has proven successful in demonstrating that Oligochaeta

are destined for a fate similar to that suggested above

for the paraphyletic Polychaeta, principally because leeches

and their allies group inside of oligochaetes.

Like earthworms, leeches are clitellates but with special

adaptations to blood-feeding. They have a muscular caudal

sucker made up of the last seven somites of the segmented

body that is critical for maintaining position on a host and is

used as a swimming fluke by the medicinal leeches (Hirudinidae).

The anterior six somites likewise are modified into

a region with a ventral sucker surrounding a mouth pore.

Leeches are subdivided into two basic groups based on anatomical

variations in blood-feeding mechanisms. The large,

wormlike members of Arhynchobdellida, of which Hirudo

medicinalis is typical (fig. 15.4A), have three muscular jaws

each with a row of teeth for cutting through skin into capillary-

rich tissues. In contrast, members of Rhynchobdellida,

as the name implies, have a muscular proboscis to effect

blood-feeding from vascularized deeper tissues.

Blood-feeding arhynchobdellids include the aquatic Hirudinidae

(“medicinal leeches”) and the terrestrial Haemadipsidae

(“jungle leeches”). The European medicinal leech has

for centuries been used in phlebotomy (blood-letting) in a

variety of regions, including China (in Wang Chung’s Lun

Hкng, circa 30 A.D.), India (in Kunja Lal Sharma’s Su’sruta

Samhitб, circa 200 A.D.), ancient Rome (in Pliny’s Natural

History, circa 50 A.D.), and throughout Europe (Shipley 1927).

Use in Europe, however, reached its peak in the 19th century

after the ascendancy of Napoleon’s army surgeon Broussais

and his student Broussard, known together as the “Grand

Sangeurs.” Leeching was a dubious cure considered for everything

from simple headaches and insomnia to ulcers and

obesity. Nonetheless, harvesting leeches from European lakes

and ponds continued intensively, with importations in the

1830s to France exceeding 50 million annually (and that notwithstanding

a duty of 1 franc per thousand). France was

hardly alone in this endeavor—Russia and Hungary each

imposed hefty export duties and fines for trafficking in the

worms, and more than seven million leeches per year were

used in London hospitals as late as 1863 (see Sawyer 1981,

Elliott and Tullett 1984, 1992).

The consequences of this demand for Hirudo medicinalis

have been profound. As early as 1823, the Hanover government

acted to restrict trade in light of declining numbers,

forbidding all exports. Sardinia followed suit in 1828 and

eventually Moldavia, Wallachia, Spain, Portugal, Bohemia,

and Italy had either exhausted populations or had banned

their export so as to conserve what was left (Sawyer 1981).

By the 1990s, Hirudo medicinalis was declared either threatened

or endangered in more than 15 countries, had been

included in the IUCN Invertebrate Red Data Book (1983), and

was listed as Appendix II in CITES (Wells et al. 1983, Elliott

and Tullett 1992).

In tropical wet forests, haemadipsids are more frequently

encountered than are hirudinids (fig. 15.6). Both of these

groups are equipped with a parabolic arc of 10 eyespots that

permit the detection of contrasting movement in three dimensions.

Haemadipsids have an unusual biogeographic

distribution, being found only on the Indian subcontinent

and in Southeast Asia, Wallacea, Australia, Melanesia, Madagascar,

and the Seychelles, but not in Africa or in South

America. All other leech families have a global distribution.

No other group of leeches has inspired such passionate accounts

by travelers or naturalists. Even North America’s most

prolific hirudinologist was particularly awestruck by this family

where, in the “dank tropical jungles, the misty ravines and the

showery, forested mountain-sides of this extensive region they

are among the most dominant and self-assertive elements”

(Moore 1927: 224). “Leeches swarmed with incredible profusion

. . . they got into my hair, hung from my eyelids and

crawled up my back” [Himalayan Journals (Hooker 1854)].

They were “so close together that your eyes had to be focused

at your feet to find a place where you could step . . . I finally

compromised with the leeches . . . letting them get their fill

. . . so long as they kept away from my face and the fly of my

trousers” [Burma Surgeon Returns (Seagrave 1946)].

Terrestrial leeches have the additional adaptation of respiratory

auricles near their caudal sucker, allowing for gas

exchange without excessive loss of fluid. Moreover, they have

well-developed sensory systems probably for detecting vibra-

Figure 15.4. (A) Hirudo medicinalis, the European medicinal

leech. Photo by M. Siddall. (B) Glossiphoniid leeches such as

Placobdelloides jaegerskeoldi exhibit a strong degree of parental

care by brooding their young. Photo by J. Oosthuizen

(deceased).

A

B

242 The Relationships of Animals: Lophotrochozoans

tions, carbon dioxide, and heat. The terrestrial habits and the

nature of the global distribution of the haemadipsids have

been cause for speculation regarding their evolutionary

history. Considerably distantly related terrestrial bloodfeeders

such as Mesobdella gemmata in Chile (Blanchard

1893), Malagobdella species in Madagascar (Blanchard 1917),

and the Seychellian Idiobdella species (Harding 1913) naturally

caused some consternation for Autrum (1939) in his

attempt to explain the world’s distribution of this group.

The two groups of proboscis-bearing Rhynchobdellida

have pairs of centrally arranged eyespots that sense at least twodimensional

movement. The small fish leeches, or Piscicolidae,

exhibit a form of parental care that promotes their offspring

achieving an early blood meal. Rather than abandoning a secreted

“cocoon” on shore, as the arhynchobdellids do, the

piscicolids cement dozens of egg cases to the surface of shrimp

or crabs. When that crustacean is eaten by a fish, juvenile

leeches jump off, attaching to the buccal surfaces or migrating

to the gills in order to acquire a blood meal. The Glossiphoniidae,

such as Haementeria ghilianii, are broad and flattened,

normally feeding on turtles or amphibians. Glossiphoniids

secrete a membranous bag to hold their eggs on their underside.

Covering their eggs (fig. 15.4B), adults will fan the brood

until they hatch. The brood then will turn and attach to the

venter of their parent, and when the parent finds its next blood

meal, they are carried to their first.

Leeches have gained importance not only in terms of their

use in microsurgery but also in relation to the isolation of

bioactive compounds from their saliva. Vertebrate blood has

a plethora of coagulation factors, and a leech ill-equipped for

preventing the activation of this system would surely perish.

Most leeches need to feed for 20–40 minutes, but blood

can clot in much less time. Should the ingested blood-meal

coagulate in their gut, this would render mating, avoidance

of predators, or seeking another meal quite impossible.

Leeches not only have dramatically circumvented the end

points of the mammalian coagulation cascade (cross-linkage

of platelets, thrombin’s production of a fibrin matrix, and the

cross-linking of that matrix into a hard clot) but also have

interfered with no fewer than seven points in the mammalian

clotting system. Hirudin, a potent thrombin inhibitor,

was the first anticoagulant to be isolated from a leech. Most

other leech-derived anticoagulants also are protease inhibitors

(of killikrein, fibrinogen, or factors Xa and XIIIa; Chopin

et al. 2000). Calin blocks von Willebrandt’s factor and platelet

aggregation. Platelet aggregation inhibitors from North

American species of Macrobdella and Placobdella (decorsin

and ornatin, respectively) block the IIb/IIIa site (Seymour

et al. 1990, Mazur et al. 1991). Yet, the most frequently discovered

anticoagulants are protease inhibitors that block

factor Xa, thus preventing conversion of prothrombin to

thrombin and that also seem to have an ability to prevent

tumor metastasis (Brankamp et al. 1990, Blakenship et al.

1990). Beyond simply stopping the formation of clots, the

giant Amazonian leech Haementeria ghilianii has also evolved

ways to break them down (Budzynski et al. 1981, Malinconico

et al. 1984). There even are known anti-inflammatory

agents such as eglin, bdellin, and cytin that have been isolated

from leeches.

Many leeches do not feed on blood at all. Glossiphoniids,

such as species of Helobdella and Glossiphonia, feed on aquatic

oligochaetes and snails. The jawless Erpobdellidae members

feed on chironomid larvae, and the jawed members of

Haempidae consume whole earthworms, shredding them

over jaws with two rows of large teeth. In addition, there

are rarely encountered families such as the South American

Americobdellidae and Cylicobdellidae that are terrestrial

earthworm hunters and of uncertain phylogenetic

affinities. Typically, it has been assumed that non-bloodfeeding

varieties are more primitive than those with the

“advanced” behavior of blood-feeding.

In addition to Oligochaeta and Hirudinea, two other

groups of annelids possess a clitellum and are included in

Clitellata: the orders Branchiobdellida and Acanthobdellida.

Branchiobdellidans, commonly known as crayfish worms, as

the name implies, are ectoparasitic of astacoid crayfish (Crustacea:

Astacidae) and are endemic to the Holarctic (Eurasia and

North America) region. They are subdivided into five families

consisting of 21 genera and approximately 150 species and

have a constant number of 15 body segments (somites). The

first four constitute the head region, with the first somite forming

an adhesive oral surface around the mouth. The last segment

forms a posterior disk-shaped attachment organ (Gelder

et al. 1988). Branchiobdellidans possess a dorsal and ventral

denticulate jaw (Odier 1823) and, like leeches, lack hairlike

chaetae. The second group, monotypic with Acanthobdella

peledina Grube 1851, is specifically parasitic on salmon and

also endemic to the Holarctic. Acanthobdella is characterized

by a constant number of 29 somites, an anterior sucker composed

of the first five somites, with hooklike chaetae limited

to this region, and a posterior sucker.

Resolution of the evolutionary lineages and relationships

among subgroups within Clitellata has been a topic of debate

deliberated for more than a century (Odier 1823, Vejdowsky

1884, Livanow 1906, 1931, Sawyer 1986, Brinkhurst and

Gelder 1989, Siddall and Burreson 1996, Brinkhurst 1999,

Siddall et al. 2002). A close relationship between branchiobdellidans

and leeches, with Acanthobdella as their sister taxon and

with the lumbriculids as a linkage between these and the rest

of Oligochaeta, has long been suspected (Odier 1823, Livanow

1906, 1931, Sawyer 1986). Before the advent of molecular

phylogenetics, these studies used morphology to discern relationships

among the groups, but because of subjective interpretations

of clitellate anatomy, agreement and resolution

of the classification have been problematic.

In particular, the taxonomic position of branchiobdellidans

and Acanthobdella within Clitellata has been problematic because

of their possession of combinations, or “transitional”

(Holt 1965, Purschke et al. 1993) forms, of hirudinean (leech)

and/or oligochaete characters. Odier (1823) and Livanow

Toward a Tree of Life for Annelida 243

(1906) hypothesized that a common ancestor existed for

these worms and leeches based on their possession of “leechlike”

characters: an attachment organ, loss of chaetae, constant

number of body segments, and an ectocommensal life

history strategy. Michaelsen (1919) was first to counter this

view, arguing that because Acanthobdella possessed cephalic

(head) chaetae and an oligochaete-type seminal funnel, it

should fall within Oligochaeta. He therefore attributed the

leechlike characters to convergence, or independent evolution,

because of the adoption of an ectocommensalistic lifestyle.

Livanow (1931) later reiterated his contention that

Acanthobdella and branchiobdellidans are more closely related

to leeches. Contrary to Holt (1965), who denied that Branchiobdellida

and Acanthobdella are phylogenetically associated

with leeches, Sawyer (1986) proposed four subclasses grouping

all of the ectocommensal clitellates as subclasses of

Hirudinea, with the inclusion of agriodrilidans (carnivorous

lumbriculids proposed to be ancestral to leeches). Holt

(1989) countered this, again affirming that the only common

characteristic was their possession of a clitellum and

that the remaining similarities must be convergences due

to ectocommensalism.

The reinvestigation of the systematic position and synapomorphies

(shared derived characters) of various annelids with

leeches continued. Several studies dismissed the obvious similarities

(Holt 1989, Brinkhurst and Gelder 1989, Purschke

et al. 1993, Brinkhurst 1994), despite phylogenetic results

corroborating various synapomorphies. Purschke et al. (1993)

and Brinkhurst (1994), for example, reexamined the morphology

of Acanthobdella and branchiobdellidans by reconstructing

cladograms that showed their monophyly with leeches and

a lumbriculid sister group. In each case they rejected their own

findings. Brinkhurst and Gelder (1989) argued that the variability

in the number of somites (hirudinids, branchiobdellidans,

and Acanthobdella have 34, 15, and 27, respectively)

was evidence of nonhomology of having a fixed number of

segments, unlike the variable number in oligochaetes. Additionally,

the presence or absence of chaetae is not consistent,

being absent both in leeches and in branchiobdellidans but

limited to the cephalic (head) region in Acanthobdella. In

comparison to lumbriculids, the coelom (fluid-filled body

cavity) in branchiobdellidans is reduced in the extremities

where muscles are well developed, whereas in leeches and

Acanthobdella it is completely reduced, with only the latter

retaining septa (coelomic tissue walls between somites). A

muscular posterior sucker, absent in oligochaetes but present

in leeches and Acanthobdella, has been referred to as a nonmuscular

“attachment disk” with supposedly nonhomologous

adhesive secretions or a “duo-adhesive” organ in branchiobdellidans

(Weigl 1994, Gelder and Rowe 1988), suggesting the

latter is not a sucker per se. Based on the lack of precise correspondence

of morphology—the basis of monophyly among

branchiobdellidans, Acanthobdella, leeches, and therefore

lumbriculid oligochaetes—the hypothesis of convergent evolution

still remained (Brinkhurst 1999).

Inasmuch as overall morphological similarities appeared

to be inconclusive, sperm ultrastructure had also been used

for phylogenetic analysis (Franzйn 1991, Ferraguti and

Ersйus 1999). Although this offered a different perspective

and broadened the basis in assessing relationships, it did not

provide conclusive resolution. Ferraguti and Ersйus (1999)

presented synapomorphies in sperm structure corroborating

the sister-group relationship of leeches and Acanthobdella,

but they found no evidence in support of an exact position

for Branchiobdella within Clitellata.

Conversely, a reconstruction of leech phylogeny based

on morphology (Siddall and Burreson 1995) seemed to be

in agreement, proposing several speculative evolutionary

relationships. Because Acanthobdella does not directly feed

on blood from the host, feeding mostly on dermal tissue, they

hypothesized that the common ancestor of leeches was in

fact not a blood-feeder and, as Sawyer (1986) proposed,

that blood-feeding was acquired independently in rhynchobdellids

and arynchobdellids. Avoiding the discrepancies

caused by conflicting interpretations of morphology and

in response to the broad convergence argued by Brinkhurst

(1994) and Purschke et al. (1993), Siddall and Burreson

(1996) took a different approach by examining the evolution

of life history strategies of leeches in contrast to oligochaete

plesiotypic (ancestral) conditions. In all cases, Acanthobdella

and Branchiobdellida retained “oligochaete” conditions with

these states being inherited by the hirudinids and later modified

into conditions more typical of leeches, which Siddall

and Burreson (1996) took as affirmation of the inclusion of

these three groups within Oligochaeta.

Since the mid-1990s, the collection and addition of

molecular data to known annelid morphology, ecology, and

life histories (within and among various groups) began to

shed light on resolving higher level relationships of leeches

down to family-level phylogenies. Siddall and Burreson

(1998) investigated the molecular phylogenetic relationships

of leeches for the first time, using mitochondrial cytochrome

c oxidase subunit I (mtCOI). This preliminary study confirmed

previously suspected internal relationships but also

suggested the existence of a sister-group relationship between

the piscicolids (fish leeches) and Arhynchobdellida. Additionally,

Oligochaeta seemed to be paraphyletic, with a split of

lumbriculids from the rest of the oligochaetes, followed by a

divergence of subsequent clitellate taxa (i.e., Acanthobdellida,

Branchiobdellida, and Hirudinida, respectively). Since then,

the use of a combination of ribosomal and mitochondrial gene

sequences with morphological data has successfully been employed

(fig. 15.5) to resolve family, genus, and higher level taxa

in leeches (Apakupakul et al. 1999, Light and Siddall 1999,

Siddall 2002, Siddall and Borda 2002).

In the same way that interpretations of morphology created

a platform for debates, conflicting results were also noted

using molecular data because of low or uneven taxon sampling

and different methods of data analysis. Martin et al.

(2000) examined the phylogenetic relationships of Clitellata

244 The Relationships of Animals: Lophotrochozoans

with maximum likelihood using 18S rRNA and mtCOI, in

separate and combined analysis. They reported that, although

their data suggested that leeches and leechlike worms do in

fact fall within a paraphyletic Oligochaeta, different sequencing

alignment methods gave conflicting results, and resolution

of Clitellata was deemed to be confounded by faster

evolving lineages.

At the 1994 International Meeting of Aquatic Oligochaete

Biology, Siddall, Burreson, Coates, Erseus, and Gelder

agreed on which genes would be pursued in order to finally

solve the question of clitellate relationships: mtCOI and 18S

rDNA. Commensurate with these data being gathered for

leeches (Apakupakul et al. 1999), substantial members of

aquatic oligochaetes had been similarly analyzed (Nylander

et al. 1998, Ersйus et al. 1999), with the attendant discovery

that Naididae and Tubificidae are in dire need of revision.

Once these data were complete for Branchiobdellida

(see Gelder and Siddall 2001), it was possible to combine all

in a broad assessment of clitellate relationships some eight

years after the authors had agreed to do so. Nuclear 18S

rDNA and mtCOI data for a total of 101 annelids were analyzed

(Siddall et al. 2002), excluding morphological data so

as to eliminate the criticism that results would be influenced

by morphological convergence. The results of this cooperative

phylogenetic work was the unambiguous validation

of Livanow’s (1906, 1931) assertions that branchiobdellidans

and Acanthobdella share a recent common ancestor

with leeches, which together form the sister lineage to the

lumbriculid oligochaetes (fig. 15.6).

Although results so far are compelling, there is still considerable

work to be accomplished among clitellate lineages.

Most notable is our relative lack of megadrile oligochaetes

such as the earthworm and allied taxa. Incorporating these

families will require considerable fieldwork acquiring fresh

specimens, particularly from South America, Africa, and Asia.

Primacy for Polychaetes

Polychaetes are generally small and cryptic. However, if one

deliberately seeks them, for example, in a grab of marine

sediment hauled up from a few hundred meters’ depth, the

number and variety of polychaetes can be overwhelming, and

it may take weeks of work to identify them. Apart from the

impact of polychaete diversity on specialists, there are a number

of ways in which polychaetes do impinge on general

human awareness.

One of the few annelids regularly eaten by people is the

palolo worm (Palola viridis). Palola viridis is a eunicid polychaete

with robust jaws that it uses to burrow through coral,

where they form large galleries. Periodically, and usually at

night, the posterior ends of these worms, about 20 cm long

and filled with eggs or sperm, detach and swim toward the

sea surface. There, people gather the worms, greatly regarded

as a delicacy. The name “palolo” is Samoan, and in Samoa

there are two breeding events, during the third quarter of the

moon in both October and November. There are a number

of Palola species around the world, including the Mediterranean

and off California, that are also known to swarm

(Fauchald 1992). Samoans and other South Pacific peoples

for centuries have known of a relationship between the emergence

of the worms, the “palolo risings,” and the phase of

the moon, now regarded as a classic example of lunar periodicity

in animals (Caspers 1984, Fauchald 1992). The anterior

end of the worm survives the spawning event and

grows a new posterior to spawn again.

Figure 15.5. Phylogenetic relationships of the principal families

of leeches based on morphological data, 18S rDNA, and 28S

rDNA, as well as mtCOI and mitochondrial 12S rDNA.

Figure 15.6. Phylogeny of the Clitellata based on a coordinated

approach from several labs using nuclear and mitochondrial

gene sequences. Oligochaetous lineages are represented by

thicker lines. Leech taxa are italicized. Based on combined

information from Siddall et al. (2001), Ersйus et al. (2000), and

B. Jameison (unpubl. obs.).

Americobdellidae

Cylicobdellidae

Macrobdellidae

Xerobdellidae

Hirudinidae

Haemopidae

Erpobdellidae

Haemadipsidae

Piscicolidae

Glossiphoniidae

Hirudiniformes

Erpobdelliformes

Piscicolidae

Glossiphoniidae

Branchiobdellida

Acanthobdellida

Lumbriculida

Tubificida

Lumbricida

Enchytraeidae

Megascolescidae

Ocnerodrilidae

Glossoscolescidae

Toward a Tree of Life for Annelida 245

Swarming of annelids occurs in other parts of the world,

and a number of different kinds of polychaete engage in this

behavior. The phenomenon is broadly known as epitoky.

Those with schizogamous epitoky, such as the palolo worm,

detach their gamete-filled posteriors and live to breed another

day. Others with epigamous epitoky, mostly in the Nereididae,

transform their bodies entirely to allow them to swim

up to the surface (e.g., by producing enlarged eyes, special

paddle chaetae, and major muscle development). After

spawning, the worms cannot possibly return to their life

on the bottom and so die. Other annelids have epigamous

epitoky but survive to breed again. The most famous of

these is the syllid Odontosyllis enopla, also known as the “Bermudian

fireworm” because their swarming is associated with

a bright green luminescence. These 1–cm-long worms swarm

in vast numbers in the evenings just after the full moons of

June and July and create luminescent displays thought to help

them attract mates near the surface of the water. After spawning,

the worms descend to the bottom again and resume their

lives (Fischer and Fischer 1995). It has been suggested that

the light Christopher Columbus described the evening before

his landfall in the Caribbean in October 1492 may have

been the glow of Odontosyllis swarms (Crawshay 1935).

Annelids have direct economic importance to human society

through their ecological function in the creation and

maintenance of marine and terrestrial soils and sediments.

Some people also make their livelihood from worms, supplying

them as bait for recreational fishing. Marine worms

in groups such as Arenicolidae, Glyceridae, Eunicidae,

Nephtyidae, Nereididae, and Onuphidae are used as bait,

whether caught in the wild or farmed in aquaculture systems.

For instance, the glycerid Glycera dibranchiata and nereidid

Nereis virens are manually harvested from mud flats of Maine

with a wholesale value of several million U.S. dollars (Olive

1994). In Europe and Asia there are several commercial worm

farms that supply tons of worms to the fishing industry (Olive

1994). At present this does not compare with the amount

harvested from the wild, with all its attendant potential degradation

of habitat.

Two polychaete groups one must be careful of are Amphinomida

and Glyceridae. Amphinomids, commonly referred to

as fireworms, induce a burning pain on anyone foolish enough

to pick them up. Commonly found under rubble in coral

reef environments, large (15–20 cm) amphinomids such as

Eurythoe and Hermodice have elongate pink or green bodies

with tufts of white chaetae emerging dorsally. These chaetae

are unusually brittle and thin and may break off in the skin,

producing an intense itchy or burning sensation that may last

for days (Kem 1988). Members of Glyceridae can reach 40 cm

in length and have four jaws at the end of their eversible proboscis,

each armed with a venom gland. They inject this venom

into their prey (crustaceans and other annelids), inducing

paralysis (Kem 1988). People who have been bitten by these

worms have reported intense pain and swelling, although there

have apparently been no deaths to date.

Alvinellidae (“Pompeii worms” and “Palm worms”) are a

relatively recently discovered annelid group known only from

sites associated with deep-sea hydrothermal vents in the

Pacific Ocean. Given this recent discovery, they are surprisingly

well studied, particularly Alvinella pompejana

(Desbruyиres and Laubier 1980, Desbruyиres et al. 1998).

Tolerating some of the most extreme living conditions of any

animal, they are called Pompeii worms because they live in

tubes on the sulfide chimney walls of active hydrothermal

vents. As such, they are continuously in the presence of an

unrelenting downpour of mineral particles that result from

fluctuating thermal and chemical reactions of the hydrothermal

fluid and surrounding seawater. Worms have been recorded

crawling at temperatures exceeding 100°C! Only the

crushing pressure of 250 atmospheres keeps the surrounding

water from boiling. Desbruyиres and Toulmond (1998)

recently described an extraordinary new hesionid polychaete

Sirsoe methanicola (as Hesiocaeca; see Pleijel 1998) living

in large numbers on frozen methane hydrate mounds associated

with cold methane “seeps” in the Gulf of Mexico

(Fisher at al. 2000). This animal is also known as the “iceworm,”

but thus far little is known about its biology.

The broad-level systematics of polychaetes, after a period

of relative stability, is undergoing major reassessment. The most

recent comprehensive systematization of polychaetes was proposed

by Rouse and Fauchald (1997) based on a series of morphological

cladistic analyses. Allowing for the likely errors in

the placement of many taxa, and the fact that there were conflicting

results included in the original analyses by Rouse and

Fauchald (1997), the most fundamental problem inherent in

their systematization may be that of the placement of the root

for any tree of Annelida. This has major implications for the

taxon Clitellata (which is now synonymous with Oligochaeta)

and the name Polychaeta itself, which may become synonymous

with Annelida. Rouse and Fauchald (1997) assessed the monophyly

of Polychaeta and relationships among the taxa usually

included in the group and those traditionally excluded. Polychaete

“families” and groups such as Sipuncula, Echiura,

Clitellata, Pogonophora, and Vestimentifera were used as terminal

taxa, largely because this allowed the most heuristic assessment

of relationships based on present knowledge. It also

permitted many of the current problems in the systematics of

polychaetes to be highlighted. They found that the traditionally

formulated Annelida were monophyletic and comprised

two clades, Clitellata and Polychaeta, although the monophyly

of the latter was not well supported at all, which is not that surprising,

given the tremendous diversity of the group (fig. 15.7).

There was no obvious sister group for Clitellata within

Polychaeta that could be identified on current morphological

evidence. Rouse and Fauchald (1997) then presented a new

classification of polychaetes based on one of the analyses.

Rouse and Fauchald (1997), Pleijel and Dahlgren (1998)

and most previous influential systematizations of polychaetes

(e.g., Fauchald 1977) recognize a taxon Phyllodocida,

explicitly or implicitly accepting that this is a clade. Basal

246 The Relationships of Animals: Lophotrochozoans

annelids, according to Rouse and Fauchald (1997), are taxa

such as Clitellata and simple-bodied polychaete groups like

Questa and Paraonidae. This rooting of Annelida was based

on outgroup choices such as Mollusca and Sipuncula and

may well be misleading. There currently is little evidence that

is not ad hoc to justify other ways of rooting this tree with

morphological data. However, several of the alternative hypotheses

(e.g., Westheide 1997, Conway Morris and Peel

1995) are similar in that they suggest that the root for the

annelid tree should be placed within Phyllodocida or

Aciculata (Phyllodocida plus Eunicida).

In addition to the rooting problem, the phenomenon of

paraphyletic taxa in polychaete systematics may be a common

situation for several reasons. Most polychaete taxa have

been named without reference to any tree topology. Classifications

based only on similarity will inevitably lead to

paraphyly. In their review of those polychaete taxa with a

rank of family, Fauchald and Rouse (1997) found that of the

80 families that they accepted as “valid,” they could provide

no evidence of monophyly for 21, including such wellknown

taxa as Eunicidae and Polynoidae. It should be noted

that even where Fauchald and Rouse (1997) suggested fea-

Figure 15.7. The anatomical

diversity of polychaetes is

tremendous, as is demonstrated

in this sampling. (A) Acrocirrus

validus (Acrocirridae).

(B) Cirratulus (Cirratulidae).

(C) Pseudopotamilla reniformis

(Sabellidae). (D) Terebellides

stroemi (Trichobranchidae).

(E) Chloeia (Amphinomidae).

(F) Eulalia (Phyllodocidae).

(G) Notomastus (Capitellidae).

(H) Nereimyra punctata

(Hesionidae). All photos by

G. Rouse.

Toward a Tree of Life for Annelida 247

tures that provided evidence of monophyly for the remaining

59 families, this must be regarded as provisional. Until comprehensive

detailed cladistic analyses are performed across

relevant sets of taxa such assumptions of monophyly for these

groups probably are unfounded. For example, Fauchald and

Rouse (1997) provided apomorphies supporting the monophyly

of Spionidae, of Longosomatidae, of Poecilochaetidae,

of Trochochaetidae, and of Uncispionidae. Subsequently, a

cladistic analysis by Blake and Arnofsky (1997) showed that

Spionidae was rendered paraphyletic relative to the other four,

which should now be regarded as junior synonyms.

Within the numerous polychaete taxa, there have also been

few detailed systematic studies. Rouse and Pleijel (2001) found

that there have been cladistic analyses only of the following

polychaete taxa: Opheliidae, Orbiniidae, Questa, Eunicida,

Dorvilleidae, Onuphidae, Chrysopetalidae, Hesionidae, Namanereidinae

(in Nereididae), Pilargidae, Syllidae, Phyllodocidae,

Notophyllum (in Phyllodocidae), Phyllodoce (in Phyllodocidae),

Glyceriformia, Sabellidae, Serpulidae, Siboglinidae, Terebelliformia,

Terebellinae (Terebellidae), and Spionidae. Clearly,

there is much work to be done toward our basic understanding

of the relationships among polychaetes.

At an even more fundamental level, it is certain that there

are many more polychaetes to be described and that they

represent an important component of the diversity of marine

animals. This is exemplified by studies on the variety of

polychaetes in a small area. In a well-known example, Grassle

(1973) found 1441 polychaetes in a single chunk of coral

weighing a few kilograms. He placed these polychaetes into

103 nominal species and noted that they represented twothirds

of the macrofauna collected. More recent surveys on

diversity of deep-sea polychaetes have shown a similar pattern:

dominance in terms of individuals and taxa (e.g., Grassle

and Maciolek 1992). What is more striking about these surveys

is the number of undescribed polychaetes that were

found (e.g., 64% by Grassle and Maciolek 1992). Arguably,

we will not arrive at a comprehensive understanding of annelid

origins and phylogeny until more of extant polychaete

diversity is found and described.

Quo Vadimus?

Certainly there has been no lack of effort regarding the morphological

characterization of annelidan groups on a broad

scale (e.g., Rouse and Fauchald 1997, Siddall and Burreson

1995, Purschke et al. 1993, Brinkhurst 1994, 1999). Homologizing

those characters and states among disparate subsets

of worms has proven more difficult and often an intractable

task for lack of independent corroboration of sister-group

relationships. Although the use of molecular sequence data

provides an opportunity to achieve those aims, there has yet

to be either a full accounting of which loci are available across

the phylum or, more importantly, what information those

data together might provide regarding support for group

membership. Currently, there are about 800 gene sequences,

divided into roughly one-third from polychaetes and twothirds

from clitellates (of which more than half are from

leeches alone). Sampling has yet to be coordinated among

various laboratories, but it can be and should start with the

complete amalgamation of sequences in a data set of approximately

365 taxa and about 4000 sites newly aligned and

analyzed. Our expectation for wholly sensible results from

that are, however, rather low. We estimate that more than

two-thirds of the preliminary matrix will be missing for lack

of overlap in data across taxa. Still, that work would create a

springboard from which several labs cooperating internationally

(Australia, France, and the United States of America)

might focus sequencing efforts on existing DNA isolates or

samples in a way that would most efficiently ameliorate topological

instability. This first phase might take less than two

years to bring to completion. A more full accounting of annelid

phylogeny will need another complementary approach

and considerably more time.

The main questions that need answers include the following:

Where does the root for Annelida lie?

What is the sister group to Clitellata?

Do other major taxa, such as Brachiopoda, Echiura,

and Sipunculida, to name a few, belong within

Annelida or are they sister to it?

These broad questions all are interlinked and, once satisfactorily

resolved, will allow for a multitude of more detailed

analyses among less inclusive annelid groups. How would

one best approach these questions, given the equivocal results

to date? The answer is, of course, more data, and lots

of it. This first means an extensive array of gene sequence

data for many terminals. The genes to be sequenced would

comprise parts of both nuclear and mitochondrial genomes.

To make the most of the data available already, these arguably

would be four nuclear regions—SSU rDNA (18S), large

subunit rDNA (28S), histone H3, elongation factor EF-1a—

plus the mtCOI and mitochondrial 16S regions. Additionally,

the sequenced specimens should be studied with a range

of morphological techniques. This would then allow for a

fuller development of the morphological data set presented

in Rouse and Fauchald (1997). Much of the data used in that

study was based on observations more than a century old,

and there are many gaps in our knowledge for many taxa.

Using light and electron microscopy of both internal and

external features, as well as larval development, a comprehensive

suite of anatomical characters could then be added

to the molecular data set. A sound tree at this level will provide

the basis for resolving many other problems in annelid

systematics. The homology of many body regions in annelids

is unresolved, and this is reflected in the multitude of

names for the “same” parts. Simplifying terminology will

make the taxonomy of the various groups easier, allowing

many more people to study annelid systematics as a whole.

248 The Relationships of Animals: Lophotrochozoans

Moreover, the full scope of diversification of life-history roles

and the phylum’s expansion across the planet in space and time

could then be understood. Our understanding of fundamental

questions such as the evolution of reproductive mechanisms,

feeding strategies, and physiology can only be enhanced

with a better understanding of annelid evolution. In the next

five years we predict it will truly be the worms’ turn.

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