Choanoflagellates FS07030

Leadbeater, B. & Kelly, M (2001).

Evolution of animals – choanoflagellates and sponges.

Water and Atmosphere Online. 9 (2): 9-11.

Reproduced with permission of Cathy Kilroy, Editor, Water & Atmosphere, Nov 2003.

9

N I W A W A T E R & A T M O S P H E R E 9 ( 2 ) 2 0 0 1

THE NINETEENTH CENTURY was rich inscientific achievements. Possibly the mostimportant of these to biology was the establishmentof evolutionary theory. Darwin’s five-year voyageon board the Beagle (1831–36) and his subsequentpublication of “The Origin of Species” (1859)promoted a fundamental explanation of howanimals and plants had evolved. The main ideawas that all life had a common origin and thatcomplex multicellular animals and plants werederived from single-celled creatures. This setbiologists in search of so-called missing linksbetween the major living groups of animals andplants. The search led to the discovery of “livingfossils” – remnant species of much larger groupsof animals or plants which had previouslydominated life on earth.

Over 140 years on, the origin of animals is stillelusive, even with the recent great advances inmicroscopy and molecular techniques. However,one important link – between unicellular andmulticellular animals – has been debated over thatwhole period.

It was first suggested towards the end of thenineteenth century that a group of non-pigmentedflagellates, the choanoflagellates, might be linkedto the sponges, a multicellular animal group. Thereason for suggesting this link was that thechoanoflagellate cell bears a remarkableresemblance to the so-called choanocyte cells ofsponges.

What is a choanoflagellate?The term choanoflagellate literally means collaredflagellate. This is an apt name to describe an ovoid-to-spherical cell with a single, forwardly directedflagellum surrounded by an inverted cone-shapedcollar of 30–40 tentacles. The flagellum beats witha base-to-tip undulation that creates a forwardlydirected current of water. Particles, especiallybacteria, are then sifted from the water by thecollar. Many kinds of choanoflagellates attach toa surface with a stalk.

Choanoflagellates are present in almost all aquatichabitats. They are bacteriovores – feeding mainlyon bacteria. They are a major component of theso-called microbial loop in foodwebs, where their

MARINE BIODIVERSITY

Evolution of animals –choanoflagellates and spongesBarry Leadbeater

Michelle Kelly

One aim ofbiodiversitystudies is towork out howdifferent kinds ofplants andanimals arerelated to eachother – all ofwhich is part ofthe much biggerstory ofevolution.

role is to feed on bacteria and to release inorganicnutrients back into the water.

In appearance, choanoflagellates are quite unlikeany other group of flagellates. In fact, their nearestrelatives may be parasitic single-celled animalsthat don’t have flagella at all.

Stalks, baskets and flagellaChoanoflagellate cells are distinctive and very easyto recognise. But the material covering the cellvaries considerably from species to species. Thisvariation gives clues about evolution within thechoanoflagellates and is probably responsible fortheir wide distribution.

The importance of the cell covering is partlyexplained by the function of the flagellum: it isused for feeding. If the cell is not attached to asurface, the beating flagellum propels the cellthrough the water, and feeding efficiency is muchreduced. So most cell coverings serve to attachthe cell to something. Many cell coverings aremade of organic material and come in differentshapes – small cups, long vases, long stalks. Somespecies are colonial with stalks arranged likefingers. Others without stalks form a colony inwhich the movements created by the flagella arecancelled out as each cell attempts to move in adifferent direction.

Drawing of astalked colonialchoanoflagellate

Codosiga botrytis.One cell body is

10 µm long.

Drawing ofa spherical colonialchoanoflagellateSphaeroeca lackeyi.Individual cell bodiesare 10 µm long.

Scanning electronmicrograph of the

basket-like lorica ofDiplotheca costata

(approximately12 µm long).

N I W A W A T E R & A T M O S P H E R E 9 ( 2 ) 2 0 0 1

10

Animal A eukaryotic organism that obtains itsnutrition by the ingestion of complex organicprey. (Eukaryotes have cells that contain discreteorganelles like a nucleus.) Animals range fromsingle cells to the most complex mammals,including humans.

Coelenterates A phylum of the Metazoa whichare aquatic and have a single body cavity. Theyinclude the jellyfish and Hydra.

Flagellum (plural: flagella) A whip-likeundulatory appendage used for locomotion insingle cells, and on multicellular organisms forcreating currents of water.

Flagellate A single cell bearing one or moreflagella. Most flagellates are motile for at leastpart of their life cycle.

Infusoria Literally means infusion animals:microscopic organisms that grow in organic

infusions. This term does not have a precisescientific meaning and is not generally usednowadays.

Metazoa A subkingdom of the AnimalKingdom comprising multicellular animalshaving two or more tissue layers.

Phylogenetic tree A “tree-like” illustrationshowing possible evolutionary relationshipsbetween organisms

Protozoa Single-celled organisms. Nowconsidered to be a very diverse grouping oforganisms, including single-celled plants,animals and fungi.

18s r-RNA gene The gene that codes for thesmall eukaryotic ribosomal subunit. Thisstructure occurs in all eukarytotic cells; thegene shows sufficient variation andconservativeness to be useful for determining“long-distance” evolutionary relationships.

Perhaps the most remarkable feature of somechoanoflagellates is their covering (or lorica) ofsilica strips, rather like matchsticks. The strips arearranged in a characteristic basket-like pattern.Each species has a particular lorica shape andcomposition.

Surrounding a cell with a basket creates drag,which counteracts the movement caused by theflagellum. A large basket of very thin silica stripscan cancel out movement altogether, and at thesame time help the cell to remain suspended inthe water. So these baskets have enabledchoanoflagellates to extend their habitat range tothe open ocean.

A link to sponge choanocytes?Sponges consist of a series of internal chamberslined with choanocytes (choano = collar; cyte =cell). Like choanoflagellates, each choanocytebears a collar of tentacles surrounding a singleanterior flagellum. Undulation of the flagella ofthousands of choanocytes creates a current ofwater that is drawn in from outside the animal,passes through the internal chambers and isexpelled through an exhalant opening.Choanocytes are responsible for transportingoxygen-rich water to the internal cavity of thesponge and for bringing food particles, particularlybacteria, to the surface of the collars where theycan be ingested.

Thus, choanoflagellates and sponge choanocytesare remarkably similar. The resemblance is alsostriking in many detailed ultrastructural features.But does such similarity imply an evolutionary

link between the two groups of organisms? Andwhy should this particular evolutionary link be soimportant?

The debate about spongesThe first recorded mention of a possibleevolutionary link between the choanoflagellatesand sponges dates back to the mid-nineteenthcentury. Dujardin (1841), a French biologist whowas interested in protozoa and their evolution,suggested that sponges were colonial Infusoria –the term then in use to describe microscopicorganisms. However, after introduction of the termProtozoa by the German biologist Golfuss (1817)and the subsequent exclusive use of this term byanother German scientist von Siebold (1845) forsingled-celled organisms, sponges came to be seenas the critical link between the Protozoa and morecomplex animals.

Haeckel, a controversial German biologist andpolymath of the nineteenth century, argued thatsponges should be included within the Metazoa,which according to his concept of evolutionincluded all “higher animals”. Nevertheless,Haeckel did not consider the sponges to be in thedirect line of animal evolution – a position hereserved for the coelenterates – but as a curiousside branch to the main line of animal evolution.

Haeckel’s views were hotly challenged by acontemporary British protozoologist, Saville-Kent(1880), who considered that the sponges werecolonial Protozoa derived directly from thechoanoflagellates on account of the similarity incollared cells. Kent was so persuaded by his view

Definitions (of terms in bold in the text)

ReferencesCavalier-Smith, T.(2000). Flagellatemegaevolution: thebasis for eukaryotediversification.Systematics 59: 361–391. [Special volumeon The flagellatesedited by B.S.C.Leadbeater and J.C.Green]

Darwin, C. (1859).On the origin ofspecies. John Murray,London.

Dujardin, F. (1841).Histoire Naturelle desZoophytes. Infusoires.Roret, Paris.

Golfuss, G.A. (1817).Uber dieEntwicklungsstufendes Thieres. LeonardSchrag, Nuremberg.

Saville-Kent, W.(1880–82). A manualof the infusoria. Vols1–3. David Bogue,London.

Siebold, C.T.E. von(1845). Lehrbuch ververgleichendenAnatomie derWirbellossen Thiere.In: Lehrbuch derVergleichendenAnataomie (eds:C.T.E. von Sieboldand H. Stannius. vonVeit, Berlin.

Whole mount of achoanocyte from afreshwater sponge.Note the singleanterior flagellum andthe collar of thread-liketentacles. Cell body isapproximately 6 µm.

11

N I W A W A T E R & A T M O S P H E R E 9 ( 2 ) 2 0 0 1

that when he eventually discovered a colonialchoanoflagellate he called it Proterospongia(protero = primitive or original) in the beliefthat it was the “missing link” betweenchoanoflagellates and sponges.

Since this time it has remained conventionalwisdom that the choanoflagellates and sponges areclosely related and that either this line of evolutionor an offspring gave rise to the Metazoa and theremainder of the Animal Kingdom.

Recent developmentsApart from electron microscopy, the greatcontribution of the twentieth century to ourunderstanding of evolutionary relationships hascome from molecular genetic analysis.

Drawing of Proterospongiahaeckeli, which Kent(1880–82) considered to bea missing link betweenchoanoflagellates andsponges. Colony is40–50 µm wide.

In particular, sequencing of the 18s rRNA genehas provided us with valuable data on which toconstruct phylogenetic trees. The information todate would appear to indicate that animals almostcertainly evolved from a choanoflagellateancestor (Cavalier-Smith 2000) and that thechoano-flagellates and sponges are probablysister groups with a common ancestor. ■

Barry Leadbeater is Reader in Protistology atthe University of Birmingham, UK. Hisinterests include the ultrastructure, physiologyand ecology of unicellular plankton organisms.In 2000 he spent a month at NIWA in Aucklandin collaboration with Dr Michelle Kelly Shanks,a world authority on sponges.

11