The Life of the First Vertebrates Robert W. Griffith BioScience, Vol. 44, No. 6. (Jun., 1994), pp. 408-417.

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The Life of the First Vertebrates

A novel hypothesis suggests that our earliest vertebrate ancestors m a y have spent their lives partly in fresh water and partly at sea

Robert W. Griffith
rom which invertebrate group did the first vertebrates arise? H o w did the transition from invertebrate t o vertebrate occur? Questions about the earliest vertebrates have long been among the most intriguing in zoology, not only because such questions involve our own direct ancestors but also because the origin of the vertebrates represents one of the major evolutionary jumps in animal evolution. The closest living relatives of the vertebrates are the protochordates such as the tunicates and the lancelets. Vertebrates and protochordates share the phylum Chordata. Although some controversy surrounds the issue, the ancestor of the vertebrates was probably similar in many ways t o the living lancelet a m phioxus (Jollie 1982). This ancestral chordate lacked most of the organ systems necessary for the active, sentient life that we associate with vertebrate animals (some zoologists prefer to use the term craniate when referring to vertebrates because it emphasizes those structural advancements that permitted an active life). The majo; vertebrate advancements are shown in Figure 1, which compares the morphology of amp hi ox us and of a fish. The advancements include a set of highly specialized sense organs (image-forming
Robert W. Griffithis a professor in the D~~~~~~~~~ of ~ i ~university ~ l ~ of ~ ~ ~ ~ ~ ~ h North Dart. ~ ~ ~ mouth, MA 02747. 0 1994 American Institute of Biological Sciences.

Anadromy would have placed a high selective value on sensory systems and the brain

eyes, olfactory organs, the lateral line, and various structures derived from the lateral line that are found in the inner ear), a large brain to integrate sensory information, and an arrangement of muscle blocks Did the vertebrates originate with a backbone that permits effec- in the sea or in fresh water? tive swimming. An enhanced metabolic capabil- Perhaps the single most important ity with more sophisticated circula- and most often debated question tory, respiratory, and digestive sys- concerning the origin of vertebrates tems also evolved to provide energy is whether it occurred in the sea or for a more active life. Furthermore, in fresh water. This question has the earliest vertebrates evolved the more significant implications than glomerular kidney ( a n excretory the simple salt content of the habiorgan based on microscopic tubules tat. More than 500 million years and tufts of capillaries that form ago, at the presumed time of verteurine by filtering the blood), a com- brate origins, freshwater rivers and plex endocrine system (with pitu- lakes are believed to have lacked itary, pineal, thyroid, and adrenal multicellular animals, whereas the glands), and a unique type of tis- seas already possessed a rich and sue-bone. In short, most features diverse fauna. If the vertebrates of the vertebrate body plan that even- originated in the sea, their body tually permitted the evolution of plan would have evolved in the conhumans were acquired during the texts of acute predation, competievolution of fish from ancestral chor- tion, and varied and abundant food dates. supplies. In fresh water, o n the other The most logical explanation for hand, there would have been no the origin and evolution of the vari- predators or competitors, and the ~ ous novel, complex, and seemingly dietary options would have been , t unrelated vertebrate advancements t limited to algae and other unicellut ~ - ~ ~ ~ t ~ ~ ~ h , is that they were favored by natural lar organisms. One cannot imagine selection. These features must have two more divergent stages for the

been functional, adaptive, and important from an early stage, aiding the survival and successful reproduction of the early vertebrates. They were therefore retained a n d improved through natural selection. There are two related questions that must be answered if we are to understand how these dramatic changes occurred: in what environment did the vertebrates originate, and what were the selective forces that favored the evolution of the vertebrate body plan?

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beginnings of the vertebrate evoluBUCCAL CIRRI DIVERTICULUM OR LIVER tionary play. HATSCHEKS'S PIT The living protochordate relatives of the vertebrates all live in the sea, HEEL ORGAN and there can be little doubt that the MUSCLE SEGMENTS vertebrate line is ultimately derived from marine ancestors. However, HARYNGEAL GILL because most living and fossil groups of f i s h e s i n c l u d e f r e s h w a t e r branches, it is reasonable to propose that a common ancestor of all vertebrates might have moved from the sea to fresh water. The debate over freshwater or Protochordate marine origins has historically included arguments from two sources: NARES (OLFACTION)' paleontoGgical data that tell us the MUSCLE SEGMENTS EYE (VISION) * apparent habitat of the earliest fosSPINY DORSAL F I N PINEAL GLAND * silized vertebrates and the physiolP I T U I T A R Y GLAND * SOFT DORSAL F I N BRAIN* ogy of water and salt balance in INNER EAR (EQUILIBRIUM)* BONY S C A L E S * living fishes, especially primitive GILLS I IONIC TRANSPORT & LATERAL LINE SYSTEM ' ones such as the jawless hagfish. qESPIRATlON * ) (DETECTS WATER MOVEMENT) The pre-eminent Harvard paleontologist Alfred S. Romer concluded after an extensive review that the earliest fossil fishes were from freshwater deposits ( R o m e r a n d Grove 1 9 3 5 ) . His arguments were reinforced by Homer Smith, a physiologist at New York University, who suggested that the structure of the vertebrate glomerular kidney is consistent with a freshwater origin (Smith 1932). O n the basis of these STOMACH^ GONADS ANAL FIN arguments, N. J. Berrill (1955) atswln BLADDER INTESTINE ANAL AND URlNOGENlTAL tempted to develop a comprehenGLOMERULAR KIDNEY * OPENINGS sive scenario e x ~ l a i n i" ehow the n protovertebrate could have evolved Vertebrate in fresh water. At about the same time that Berrill (1955) developed his freshwater sce- Figure 1. The morphology of the protochordate amphioxus compared with that of nario, British physiologist James D. a vertebrate, an advanced bony fish. Features o r novel uses of existing features that Robertson presented compelling ar- evolved in the early Paleozoic during the transition from protochordate t o are an asterisk. Many characteristics seen guments that vertebrates originated ancestral protovertebrate jaws,designated bythe swim bladder, and a bony internal in the bony fish, such as paired fins, in the sea (Robertson 1957). He s k e l e t o n , a r e s u b s e q u e n t e v o l u t i o n a r y a d v a n c e m e n t s n o t f o u n d in t h e noted that the blood composition of protovertebrate. Note especially the concentration of sensory and integrative the hagfish (considered the most structures in the head of the vertebrate, indicative of the phenomenon of cephalprimitive living vertebrate) points ization that provides the vertebrates with their alternate name, the craniates. Most toward a marine origin and that labeled structures around the anterior end of amphioxus, such as buccal cirri, filtration systems analogous to the Hatschek's pit, and the wheel organ, are associated with feeding. glomerular kidney of vertebrates occur in some marine invertebrates with no freshwater history. H e also leontological and physiological evi- end of the Cambrian and from the discussed accumulating paleonto- dence is beginning to erode the sup- early Ordovician periods are generlogical evidence that the earliest ver- port for a strictly marine scenario ally regarded as the oldest vertebrate fossils (Repetski 1978). The tebrate fossils were from marine for vertebrate origins. geological periods and examples of rather t h a n freshwater deposits their fauna are shown in Figure 2. (Dennison 1956). The fossil record of very The earliest traces of vertebrates are Robertson's (1957)arguments for early vertebrates sporadic and poorly characterized, the origin of vertebrates in the sea have remained largely unchallenged Small fragments of dermal bone that but Middle Ordovician vertebrates over the years. However, recent pa- occur in marine deposits from the are well known and abundant in

ll

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June 1994

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ERA
CENOZOIC

PERIOD

MlLLlONS OF YEARS B P
24

MAJOR EVENTS IN VERTEBRATE EVOLUTION

AGE O f MAMMALS DIVERSIFICATION OF MAMMALS

NEOGENE PALEOGENE
63

MESOZO'C

CRETACEOUS
138

>

AGE OF DINOSAURS

JURASSIC
205

TRIASSIC
2 40

DIVERSIFICATION OF REPTILES

PALEOZOIC

PERMIAN
290

+FIRST REPTILES
Fl RST +AMPHIBIAN5

CARBONIFEROUS
360

about their soft-bodied ancestors and where they lived. Some recent findings may shed some light on the nature of unarmored vertebrate ancestors. A fossil soft-bodied marine chordate has been described from the Middle Cambrian Burgess shale (Conway Morris and Whittington 1979). Perhaps even more relevant (and perplexing t o most vertebrate paleontologists) is recent evidence that conodonts, widespread tooth-like fossils that occur in marine deposits from the Late Cambrian until the Triassic, are from chordate, probably even vertebrate, animals (Aldridge et al. 1986, Sansom et al. 1992).

The osmoregulatory physiology of living fishes

The cells and tissue fluids of animals contain salts and other solutes that play crucial roles in metabolic processes and in muscle contraction and nerve conduction. These processes would be disrupted if solute levels were to vary much, so advanced animals usually maintain fairly constant levels of total solutes (osmotic regulation) a n d individual salts (ionic regulation). This regulation is obviously more complicated for animals that live in habitats with variable salinity or those in which the internal composition differs greatly from that of the habitat. Such animals possess specialized organs for the exchange of ions and water with the environment. These organs permit the blood's composition to be maintained. In aquatic vertebrates, there are four distinct patterns (three in the sea and one in fresh water) of regulating blood osmotic and ionic composition (Griffith 1985). These patterns of osmoregulation a n d their underlying mechanisms are shown in Figure 3. The pattern seen in freshwater fishes (blood sodium chloride levels approximately 30-40% those of seawater) is ubiquitous for vertebrates living in this medium, and, although the sites for ion uptake and water excretion differ, it also is characteristic of active freshwater invertebrates such as crayfish. The reason for this uniformity is that blood ion levels of freshwater animals are held

DEVONIAN SILURIAN ORDOVICIAN

CAMBRIAN
FIRST METAZO

PHANEROZOIC OR PRECAMBRIAN

Figure 2. The geological calendar with times of key events in the evolution of the vertebrates, as deduced from the fossil record. Representative contemporaneous animals are shown o n the right.

certain restricted localities, notably the Harding sandstone formation of Colorado. The Harding sandstone vertebrates were jawless fishes with bony shields (ostracoderms) of the genera Astraspis and Eriptychius. Until recently, they were believed to have inhabited shallow marine environments (Darby 1982) or perhaps estuaries with variable salinity (Spjeldanaes 1979). Recently, a new Harding sandstone locality has been described in which the vertebrate remains were deposited in channels of freshwater rivers (Graffin 1989). Later ostracoderm fossils from the Silurian (and various other groups of fishes that evolved during the Late Silurian and

the Devonian) are also commonly found in freshwater deposits (MoyThomas and Miles 1971, Halstead 1985).From early times, vertebrates, even individual species, appear to have been capable of living in both freshwater and marine habitats. It must be noted that the paleontological data provide only a narrow view of early vertebrate evolution. Hard tissues such as bone are usually the only evidence preserved in the fossil record; in the early ostracoderms, bone is believed to have been restricted to adults (Halstead 1973). Thus, we have n o direct fossil evidence concerning the larval development of the Harding ostracoderms, nor d o we know much

SEA WATER

(OSMOLALITY lOOOmOsm1kg Na plus CI 1000mM)

WATER

in check by two opposing selective forces. One is the need to maintain

high blood sodium for efficient operation of the nervous system, because the velocity of nerve conducWATER OSMOLALITY 400 tion depends on the cable properties Na & CI 400 AND I ) I of intra- and extracellular fluids, NaCl which are directly related to their ionic concentration. The opposing selective force is budgetary; the metabolic energy saved by having lower osmotic and ion gradients can be b WATER used for growth and reproduction. Ureosmotic Most physiologists believe that regulator those marine fish groups that dis(shark) play osmoregulatory patterns with low ion levels (hypoosmotic and Na & CI 500 ureosmotic regulators) a r e ultimately derived from ancestors who inhabited fresh water (Pang et al. 1977). This group would include the lampreys, sharks and their relac WATER tives, and all bony fishes-everyNonregulator thing but the hagfish. Regulation of (hagfish) ions a t levels lower than those of sea Na & CI 1000 water imposes a high energy cost for UREA 2 marine fishes yet confers no direct benefits. In fresh water, however, regulation of relatively low internal ion levels is adaptive:.it lowers passive water gain and salt loss. The low ion levels of most marine fishes FRESH WATER (OSMOLALITY 10 mosmlkg Na plus CI < 10mM) are thus seen as a historical conseWATER quence of resuming marine life after Hyperosmotic NaCl n a freshwater residence in which low regulator ion concentrations characteristic of (teleost) vertebrates were energetically adapOSMOLALITY 300 tive. cl In the sea, low levels of ions, although deleterious from a n energy perspective, were retained because V changes would have disrupted nerve WATER NaCl and muscle function. The shark strategy of high urea levels and the teFigure 3. The four osmoregulatory strategies of living aquatic vertebrates. a. leost strategy of low total solutes Marine teleosts have osmolality and ion levels lower than those of sea water, and are viewed a s alternative oathwavs they passively lose water and gain salts. They offset this loss by drinking and by which different fish groups kebt actively absorbing ions across the gut, which draws water inward. Excess ions are blood salt levels low when they excreted by active transport using gill chloride cells. b. Marine sharks have fluid osmolality similar t o the habitat's, so they are in osmotic equilibrium. However, reinvaded the sea from fresh water. " their ion levels are low, s o salts gained passively must be eliminated via chloride Even though such features would cells o r the rectal gland. The shark's isosmotic hypoionic status is achieved seem to be of little or no use in the through high urea levels. Because environmental urea levels are negligible, passive sea, sharks and most marine bony loss is offset by energy-requiring urea synthesis in the liver. c . The hagfish fishes have retained glomerular kidregulates neither osmolality nor major ions and is in osmotic and ionic equilibrium neys and branchial pumps for the with sea water. d. In all freshwater fishes, osmolality and ion levels exceed the active uptake of sodium and chlohabitat's, leading to passive water gain and ion loss. Ions are absorbed by active ride. In some marine teleosts, howgill uptake and, in almost all species, excess water is filtered through the glomeruli ever, the renal glomeruli have been of the kidneys, using blood pressure as the driving force. Osmolality is given in secondarily lost, and the kidneys units of milliosmoleslkg, and urea and the sum of sodium plus chloride in millimoles/kg. The sum of the concentrations of all solutes in m M usually form urine by secretion alone (Smith approximates osmolality. Passive movement of solute o r water d o w n concentra- 1 9 3 0 ) . The hagfish's maintenance of intion gradients is indicated by open arrows; active ion transport o r induced water ternal salt concentrations like those movement that requires energy by solid arrows.

Hypoosmotic regulator (teleost)

p::& 0v 3
A

June 2994

41 1

of sea water is regarded by many as a strong argument against the freshwater origin of vertebrates (Robertson 1957). Hagfish d o regulate specific ions such as calcium, phosphate, magnesium, a n d sulfate (as do marine invertebrates), but sodium and chloride are not regulated, so thev are at seawater levels. ~ a g f i s hare usually considered the most primitive living vertebrates, and nonregulation of sodium a n d chloride is unquestionably the primitive condition for marine animals because it occurs in all strictly marine invertebrates. Because blood ion levels are conservative in animals, one would expect that if hagfishes had a freshwater history their blood ions would be lower than those of sea water. The rule of parsimony supports the a r g u m e n t t h a t the hagfish's ancestors, including the first vertebrate, never occurred in fresh water. A less parsimonious alternative is that the ancestors of the hagfish lived in fresh water and regulated ions at low levels, but after becoming restricted to the marine habitat they eventually reverted to nonregulation. " Hagfish d o have several features MARINE that ;re logically linked with ion regulation o r with life in fresh water. They have glomerular kidneys that, as Smith (1932) pointed out, are admirably designed t o excrete I FRESHWATER ) large volumes of water in a dilute environment. The tubules of these Figure 4. Phylogenetic tree of the vertebrates with suggested primary environkidnevs can reabsorb sodium. also ments of various lineages. Diagrams of representative living chordates are shown useful t o freshwater animals that a t the end of each branch, and diagrams of key fossil animals (the protochordate need to conserve salts; their gills Pikea, a conodont animal, the ostracoderm Astraspis, and a jawed acanthodian) tree. Although the phylogeny and skin, like those of the ion-regu- are shown a t their aapproximate positions o n the zoologists, several points (e.g., shown here reflects consensus of many vertebrate lating fishes, are much less perme- the position of the coelacanth relative t o other jawed vertebrates and that of the able t o salts than are the e ~ i t h e l i a of hagfish a n d lamprey relative t o each other and to the jawed fishes) are currently marine invertebrates (McInerney the subjects of debate. The environmental history of most lineages of fish is 1974). Their gills have ion pumps complicated because of invasions of diverse habitats during adaptive radiations. for taking up sodium and chloride This figure depicts the suggested habitats in which the major phylogenetic groups in exchange for hydrogen and bicar- originated and the principal environment of the main ancestral line leading t o bonate ions. a feature otherwise re- extant vertebrates. stricted to freshwater animals and those derived from freshwater an- acteristic can be explained without neys that they use to get rid of metacestors (Evans 1 9 8 4 ) .Recently, hag- one's being forced to invoke a fresh- bolic waste products a n d excess fish were found to possess typical water history. These characteristics magnesium and sulfate (Potts and vertebrate chloride cells ( o r iono- would be ~ r e a d a p t a t i o n s ,serving Parry 1963), although their kidneys cytes) in their gills, cells specialized another original function in the sea are not homologous with the glomfor the outward secretion of ions in but available for use in ionic and erular kidney of vertebrates. The sea water and a true hallmark of ion osmotic regulation if fresh water hagfish's kidneys could also be used for these purposes. (Recent evidence regulation (Bartels 1985, Mallatt et were subsequently invaded. Various m a r i n e invertebrates suggests, however, that the hagfish's al. 1987). W h y should hagfish have these (e.g., mollusks, some annelids, and blood pressure is too low for the freshwater features? Each such char- arthropods) have filtration-type kid- kidney to function by filtration de412

BioScience Vol. 44 No. 6

spite its design; Riegel 1986.) The sodium-hydrogen and chloride-bicarbonate pumps could function to excrete excess acidic byproducts of metabolism rather than t o acquire ions (Evans 1984). It is possible the chloride cells are the site of branchial sodium/hydrogen and chloride1 bicarbonate exchange and hence are involved in acid and base balance (Mallat et al. 1987). I prefer the alternative explanation for the presence of glomerular kidneys a n d gill ion regulatory mechanisms in hagfish; that chloride cells and other hagfish freshwater and ion-regulatory features are largely nonfunctional historical relics of a freshwater and ion-regulatory past. Aside from its high blood ion concentrations, the hagfish's osmoregulatory features are suggestive of a freshwater ancestry, and it is not ~ a r s i m o n i o u sto shoehorn them into a strictly marine model for vertebrate origins. In what manner might hagfishes have lost ion regulation and reverted to the primitive strategy of marine nonregulation? This question is readily answered, because ion regulation is metabolically expensive. In the absence of some compelling reason to maintain low levels, natural selection favors the gradual elevation of blood ions in marine fish because the energy savings can be channeled into enhanced growth o r reproduction. However, this elevation should be gradual because ions play crucial physiological roles in nerve and muscle activity and cell biochemistry. Following the Nernst relationship (which describes the relations hi^ between ion concentrations and electrical potential across a membrane), membrane-potential changes that ~ e r m inerve conduction and muscle t contraction depend on ratios of ions, principally sodium and potassium, between the blood plasma and intracellular fluid (Withers 1 9 9 2 ) . Unless linked with a simultaneous and proportional elevation of cellular concentrations, elevating blood sodium concentrations uDsets these ratios. Because ions affect the activity of cell enzymes, changes of cellular ion levels are resisted. The com~ l e ix nteraction of ion roles in nerve and muscle function and cell bioJune 1994

chemistrv should not Drevent evolutionary ihanges in blood ion levels from occurring, but should make them occur very slowly. There are some factors in addition to enzymatic and neuromuscular functions that favor maintenance of low blood ion levels in certain marine fishes. Periodic exPosure to fresh water or very dilute seawater is a compelling reason. Low blood solutes can provide buoyancy, which helps pelagic species swim more efficiently, and low levels of blood ions make mineralization of bone easier. Hagfish lack bone, are benthic, and live in marine habitats where they are never exposed to dilute sea water, so these factors are not significant to them. Hagfish have also lived in a strictly marine environment for a long time compared with other fish groups. Although only one fossil hagfish (Carboniferous) has been described (Bardack 1985), it has been suggested that conodonts that occur in marine d e ~ o s i t s from as early as the Late Cambrian are the teeth of fossil relatives of the hagfish (Kresja et al. 1990). The hagfish is a prime candidate for reversion to ionic nonregulation. My research on the blood chemistry of marine fishes (Griffith 1981, 1985) suggests that groups with a long marine history (such as sharks and their relatives and certain deepsea bony fish) have much higher blood ion levels than fish that Dresumably branched more recently from freshwater o r euryhaline forms (i.e., inshore and neritic marine teleosts). It seems auite reasonable that the hagfish is'the extreme example of this trend.

evolved from protochordate ancestors. A good scenario should incorporate what we d o know about fossil animals and ancient environments. It should be in keeping with general biological principles derived from studies on living animals from disciplines such as ecology, physiology, functional morphology, a n d development. It should proceed in a logical manner, relying o n the rule of parsimony when in doubt. Although such hypotheses cannot be as rigorously tested by experiments as those of some other scientific fields, their ability t o parsimoniously account for the origin of the myriad novel vertebrate features can be used as a measure of their relative merits.

Marine scenarios
For more than 3 0 years. most zoologists have accepted the view of Robertson ( 1 9 5 7 ) that the vertebrates originated in the sea. Consequently, recent attempts to provide a functional explanation for the evolution of vertebrate characteristics were generally based on this premise. Although many such marine scenarios, varying in complexity and reasonableness, have been proposed over the years, the more recent, thoughtful, and comprehensive ones have a common theme: that the evolution of vertebrate features was associated with a switch from filter feeding or some other nonselective feeding mode to predation (Jollie 1982, Mallatt 1985, Northcutt and Gans 1983). ~ r e d a t i o ; requires sensory systems (eyes, lateral line organs, and olfaction) for the detection of prey, it requires a more complex brain to coordinate sensory input and learned information so that motor responses are appropriate, and it requires metabolic advancements (efficient muscle arrangement, respiration, circulation, digestion, and energy storage in the liver) to search for and catch prey. Although a switch to predation may not be the only feasible functional explanation of how vertebrates could have arisen in the sea, it certainly provides a reasonable and parsimonious scenario for the origin of many of the key vertebrate advancements.

Scenario building
Skeptics can legitimately argue that direct paleontological a n d physiological data remain ambiguous concerning the marine or freshwater origin of vertebrates and that the most parsimonious explanation remains marine. Is it possible that some indirect approach might help settle the issue? One such approach is the construction of alternate hypotheses or scenarios that attempt to explain how the vertebrates might have

The origin of vertebrate osmoregulatory features such as the kidneys, chloride cells, a n d gill ion pumps cannot be explained by marine predatory scenarios alone. Some marine proponents have suggested that the protovertebrates may not really have been strictly marine; they mav have inhabited coastal areas and estuaries of variable salinity where such osmoregulatory adaptations were useful (Northcutt and Gans 1983). Others have proposed that the original roles of ion pumps and chloride cells were to regulate acid balance, and that a buildup of acidic metabolic ~ r o d u c t scould present problems to an active predator forced to undergo anaerobic glycolysis while pursuing prey (Mallatt et al. 1987). These are plausible suggestions, but neither isconvincing. Many marine invertebrates inhabit inshore areas and even estuaries without having evolved such osmoregulatory adaptations. The h v ~ o t h e t i c a r ole of chloride cells in l s d i u m / h y d r o g e n and chloridelbicarbonate exchange has not been verified experimentally (Karnaky 1986). ~h'e presence in early ostracoderms of a shield of armor, consisting of thick plates of dermal bone that covered the head and trunk. is a particularly thorny problem to proponents of marine predator scenarios. Most zoologists believe that the bony ostracoderms were o n the main line of vertebrate evolution and that the absence of bone in living jawless fishes, lampreys, and hagfish, may be secondary (MoyThomas and Miles 1 9 7 1 ) . The use of heavy bony armor fdr obvious roles such as protection would seem to be incompatible with an active predatory life-style because it hampers mobility. O n e hypothetical function for dermal bone in early predatory vertebrates was as an adjunct to sensory systems that detected the electrical fields of prey (Northcutt and Gans 1983). This suggestion is not p a r s i m o n i o u s , because e l e c t r o reception in living fishes does not involve bone, and it has recently been s h o w n t h a t t h e p u t a t i v e electroreceptive organs in the dermal bone (cosmine) of fossil fish were really blood vessels (Bemis and 414

Northcutt 1992). Freshwater protovertebrates The recent demonstration that would have grown slowly and had conodonts (which precede ostraco- limited reproductive potential, underms in the fossil record) are com- less they migrated to nearby estuarp o s e d of e n a m e l - c o v e r e d b o n e ies and coastal marine habitats t o (Sansom et al. 1992) does lead to a feed after they had grown big enough reasonable hypothesis for the origi- to compete successfully with marine nal function of bony tissue consis- species. A strictly freshwater prototent with predation. C o n o d o n t s vertebrate makes little sense ecopresumably served as teeth that func- logically, b u t a n a d r o m y , w i t h tioned in capturing or piercing prey breeding occurring in fresh water as d o the horny teeth of hagfishes and juveniles feeding and growing and lampreys (Kresja et al. 1990). rapidly in estuaries and the sea, However, the conodont connection would have been a reasonable lifedoes not provide an explanation for style during the early Paleozoic, as it the elaboration of bony dermal ar- is today for lampreys, sturgeon, striped bass, and salmon. mor in mainline vertebrates. The anadromous lamprey is, like the hagfish, a primitive jawless fish, The anadromous scenario which lends credence to the suggesHaving concluded that the paleon- tion that the anadromous life-style tological evidence did not preclude might be original for vertebrates. a freshwater origin and that the Lampreys breed in rivers, where their physiological evidence favored some eggs develop i n t o filter-feeding freshwater involvement, I tried to ammocoete larvae (the similarity of build a scenario that explained how the lamprey ammocoete larva t o and whv marine ancestors of the amphioxus has been observed by first vertebrates might have invaded anatomy students for many years). fresh water (Griffith 1985). I sug- After metamorphosis, the juveniles gested t h a t s o m e filter-feeding of most lamprey species migrate to prevertebrate chordates invaded es- the sea, where they feed as parasites tuaries t o use t h e m a s feeding o n fishes; they return as adults to grounds, because these areas are rich fresh water to spawn. in nutrients and microscopic plants Although the parasitic habitus of and there would have been few com- the adult lamprey is likely a specialpetitors present. As a consequence, ization, the developmental pattern, these animals gradually evolved with a microphagous freshwater freshwater osmoregulatory features larva a n d macrophagous marine such as low blood ions, kidneys, and adult. makes a more reasonable branchial ion pumps to cope with model for the original vertebrate life cycle than does the direct develtheir new dilute habitat. Freshwater rivers are usually less opmental pattern of the hagfish in ~roductive than estuaries or coastal the deep sea. Those who would arseas. During the early Paleozoic, gue that the protovertebrate was when there were no multicellular marine, not anadromous, are still freshwater or terrestrial plants or left with the question of how the animals, the rivers were probably lampreys subsequently evolved their more sterile than they are today. anadromous life cvcle. In addition to making ecological Consequently, feeding would not favor movement from estuaries into sense, anadromy is compatible with the early vertebrate fossil record. fresh water. and rare distribution F r e s h w a t e r r i v e r s , h o w e v e r , The s ~ o r a d i c and would have held a decided advan- of ~ a A b r i a n Lower Ordovician tage over Paleozoic estuaries and ostracoderm fishes that have been coastal seas as safe havens for re- regarded as marine is rather what production and early development. one might expect for anadromous There were n o river vredators o r populations, not successful marine competitors, and rivers are more animals. The common Middle Orstable than estuaries in environmen- dovician Harding sandstone vertetal variables important to develop- brates were found in freshwater as ment such as salinity,. sedimenta- well as estuarinelcoastal habitats. , In Upper Silurian a n d Devonian tion, and oxygen levels. BioScience Vol. 44 No. 6

times, most extant vertebrate groups, both jawed and jawless fishes, successfully invaded freshwater environments (Halstead 1985). An anadromous history would have prepared these fishes for freshwater invasions that coincided with the proliferation of freshwater and terrestrial plants and invertebrates: they were already living there during part of their life cycle. The recent allocation of conodonts t o the vertebrate lineage (Sansom et al. 1 9 9 2 ) is compatible with marine predatory scenarios, but it is eauallv consistent with this anadromous hypothesis. I regard conodonts as fossils from an early marine branch off the anadromous lineage whose living descendent is the hagfish (see Figure 4). Reconstructions of the life of ancient conodont animals are obviously highly speculative but, if we e x t r a ~ o l a t efrom the anadromous scen&io, they would have had the capacity to regulate ions below seawater levels (I argue this capacity was lost very gradually in hagfish). Hence, the conodonts could have invaded dilute environments (they are found in Harding sandstone de~ o s i t s ) .their dilute bodv fluids hou1d"have provided them with buoyancy useful for a pelagic existence (Griffith 1981), and low ion concentrations would have facilitated the deposition of calcium phosphate in their bony teeth (Moss 1968, Nancollas and Tomazik 1974). In contrast t o marine scenarios, the anadromous scenario provides a satisfactory explanation of the osmoregulatory physiology, habitats, and life histories of virtually all living fishes. It is difficult t o generalize about the environmental history of different lineages of fish, because most groups have undergone adaptive radiations into a variety of habitats. Nevertheless, it is reasonable to suggest the following points (Figure 4):
L ,

The ancestral vertebrate was anadromous and, like most descendants, regulated ions at relatively low levels. Hagfish reverted to a fully marine life, replacing freshwater breeding and development
June 1994

with a specialized reproductive mode involving a small number of large encapsulated eggs and, although they lost ion regulation, they retain nonfunctional relics of an anadromous past in their chloride cells, kidneys, and ion uptake pumps. Lampreys remained anadromous. The ancestral jawed fish was anadromous (Griffith 1991). Sharks and ancestors of the living coelacanth became predominantly marine, evolving ureosmotic regulation. Ancestors of living lungfishes became restricted t o fresh water. Tetrapods evolved in fresh water and later invaded land. T h e rayfins (teleosts) remained euryhaline a n d exploited diverse aquatic habitats and life-styles, including anadromy. The anadromous scenario helps provide a reasonable functional explanation for the origin of bony a r m o r in the early ostracoderm fishes. We usually think of the main functions of bone as elements in lever systems that convert muscle contractions into body movements (e.g., o u r limbs, backbones, a n d jaws), as armor protecting vital organs (e.g., our skull and rib cage), or as teeth. However, bone is also a reservoir for calcium and phosphate. In humans and other terrestrial vertebrates, bone plays a vital role in the regulation of blood calcium levels. Its mineralization a n d reabsorption are under the control of hormones from the parathyroid and thyroid glands. The role of bone in calcium regulation in fishes is less crucial than in land animals, but the phosphate stores found in bone play a vital physiological role during reproduction. Fish and other lower vertebrates provide their eggs with a phosphate-rich protein, vitellin, t h a t serves as a source of building blocks for embryonic growth. Vitellin is manufactured in the mother's liver under the control of estrogen, which also induces phosphate mobilization

through bone reabsorption. The role of estrogen in vitellin synthesis is ancient in vertebrates, because it occurs in hagfish ( Y u et al. 1981) even though they have no bone to reabsorb. Most living anadromous fishes feed little during their migrations. During the early Paleozoic, when the rivers had even less food, the hypothetical anadromous ancestral vertebrates would have been unable to acquire phosphate or other minerals through the diet during their upstream spawning migrations. The c a p a c i t y of t h e f e m a l e p r o t o vertebrates to synthesize vitellin, which was vital to reproductive success, would have depended on body phosphate reservoirs that would have provided a strong selective pressure for the evolution of dermal bone as a reservoir. When I originally proposed the a n a d r o m o u s scenario (Griffith 1985), I was not thinking of the evolution of sensorv svstems and , , the brain, but it subsequently became obvious to me that anadromy would have placed a high selective value o n the d e v e l o ~ m e n tof the brain, lateral line system, eyes, and olfaction in the protovertebrate (Griffith 1987). The lateral line system of fishes is used to sense the direction of water movement from any source: from the currents of a flowing river, conspecifics swimming in a school. or the movement of predators or prey. Information about current direction is especially important to an animal living in flowing waters that needs either t o maintain its position (as d o the young of anadromous animals) or t o migrate upstream (as d o the adults during their breeding migration). The capacity to sense the direction of currents is useless for orientation without some mechanism to establish movement relative t o a fixed position in space. For bottomliving animals this capacity can be provided by contact with the substrate, but for mobile animals visual clues, such as images of rocks or other stationary objects, are necessary. (You can recognize the problem faced by a sightless anadromous fish if you imagine yourself drifting along in a river with your eyes closed. Would you be able to point up-

stream?) Eves and the lateral line , system serve together t o provide anadromous animals with the necessary information for orientation in rivers. Advanced anadromous fish such as salmon find their home streams with the aid of their sense of smell, detecting subtle differences in trace organic chemicals in water from different sources. Adult lampreys also use olfaction in their breeding migration; they seem t o respond to chemicals (pheromones) released by larval lampreys (Teeter 1980). This sort of behavior would be highly advantageous to anadromous protovertebrates (as it presumably is to lampreys), enabling potential mates t o be drawn toward the same breeding location and ensuring that breeding occurred in a habitat that could sustain the young. Given that a variety of sensory systems are required for anadromy, it follows that a well-developed brain is also necessary. Complex information from olfactory organs, eyes, and other sense organs must be interpreted in the light of past experience or innate behavioral programs, so that appropriate motor responses will occur. T h e vertebrate metabolic a d vancements in locomotion, r e s ~ i r a tion, circulation, and energy storage fit comfortably i n t o a n anadromous scenario (Griffith 1 9 8 7 ) . Upstream migrations for spawning require both sustained swimming and periodic bursts of vigorous activity to overcome obstacles such as r a ~ i d s .An efficient arrangement of swimming muscles and well-designed respiratory and circulatory systems t o deliver oxysen to the active muscles are obvi" ous prerequisites for these migrations. Storage of energy reserves in the liver and elsewhere, another vertebrate development, is also required to provide energy during m i g a t i o n s when animals are unable to obtain food. Anadromy also provides a compelling rationale for the origin of the complex vertebrate endocrine system, another set of features that evolved in the protovertebrate. Hormones secreted by the endocrine organs of living vertebrates (e.g., the pituitary, pineal, thyroid, and
, ,

adrenal glands; the gonads; and the h , ~ o t h a l a m u s )serve t o control v many physiological functions, most importantly the timing of growth, development, and reproduction. There should not be a vital need for precise endocrine timing of development and reproduction in a marine protovertebrate if, like living protochordates, it lived, fed, and reproduced in the same general area and had a protracted reproductive period. O n t h e o t h e r h a n d , a n anadromous ~ r o t o v e r t e b r a t ethat mistimed its spawning migration would run out of energy reserves, die, and leave no offspring. If juveniles migrated downstream before they were sufficiently mature, they would not survive competition and predation; if they waited too long, they would waste time in nonproductive fresh waters with lower overall reproductive success. A number of invertebrates. including insects a n d some marine taxa, do have sophisticated endocrine systems, but usually in association with complex life cycles (Withers 1992). All in all, a complicated life history such as anadromy provides a more compelling rationale for the origin of the vertebrate endocrine svstem than d o alternative marine scenarios.

Conclusions
The hypothesis that the evolution of t h e e a r l y v e r t e b r a t e s involved anadromy is ecologically plausible, consistent with the fossil record, and provides logical functional explanations for the evolution of numerous vertebrate features such as dermal bone, osmotic a n d ionic regulation, enhanced metabolic ca~ a b i l i t y ,and sophisticated sensory and central nervous systems. Alternative hypotheses that rely o n a switch from nonspecific feeding to predation in marine habitats as the force favoring the evolution of these vertebrate features are less successful in providing a comprehensive scenario for the origin of vertebrates.

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Scotland. Lethaia 19: 279-291. Bardack, D. 1985. Les premieres fossiles de hagfish Myxiniformes, e t Enteropneusta ( H e m i c h o r d a t a ) d e p o t e s d e la f a u n e (Pennsylvanienne) du Mazon Creek dans I'lllinois USA. Bulletin Trimestriel de la Societt d'Histoire Naturelle et des Anzis du Mustunz d'Autun 116: 97. Bartels, H . 1985. Assemblies of linear arrays of particles in the apical plasma membrane of mitochondria-rich cells in the gill epithelium of the Atlantic hagfish ( M y x i n e glutinosa). Anat. Rec. 2 1 1 : 229-238. Bemis, W . F., and R. G. Northcutt. 1992. Skin and blood vessels of the snout of the Australian lungfish, Neoceratodus forsteri, and their significance for interpreting the cosmine of Devonian lungfishes. Acta Zool. (Stockh.) 73: 115-139. Berrill, N. J. 1955. The Origin of Vertebrates. O x f o r d University Press, N e w York. Conway Morris, S., a n d H . B. Whittington. 1979. T h e animals of the Burgess shale. Sci. Am. 240: 122-133. Darby, D. C. 1982. T h e early vertebrate Astraspis, habitat based upon lithographic association.]. Paleontol. 56: 1187-1 196. Dennison, R. H . 1956. A review of the habitat of the earliest vertebrates. Fieldiana Geol. Mern. 11: 357-457. Evans, D. H . 1984. Gill Nat/H* a n d C1-/ HCO; exchange systems evolved before the vertebrates entered fresh water. ]. Exp. Biol. 113: 465-469. Graffin, G . W. 1989. A new locality of fossiliferous Harding sandstone: insights into the Ordovician vertebrate aquatic environment.]. Vertebr. Paleontol. 9 ( 3 ) :23A. Griffith, R. W. 1981. Composition of the blood serum of deep-sea fishes. Biol. Bull. (Woods Hole) 1 6 0 : 250-264. . 1985. Habitat, phylogeny and the evolution of osmoregulatory strategies in primitive fishes. Pages 69-80 in R. E. Foreman, A. Gorbman, J. M . Dodd, a n d R. Olsson, eds. Evolutionary Biology o f Prirnitive Fishes. Plenum, New York. . 1987. Freshwater or marine origin of the vertebrates? Conrp. Biochem. Physiol. 87A: 523-531. . 1991. Guppies, toadfish, lungfish, coelacanths and frogs: a scenario for the evolution of urea retention in fishes. Environ. Biol. Fishes 32: 199-21 8. Halstead, L. B. 1 9 7 3 . The heterostracan fishes. Biol. Rev. Cafnb. Philos. Soc. 48: 279-332. . 1985. The vertebrate invasion of fresh water. Philos. Trans. R. Soc. Lond. B Biol. Sci. 309B: 289-322. Jollie, M. 1 9 8 2 . W h a t are t h e "calcichordata"? a n d the larger question of the origin of the chordates. Zool. I. Linn. Soc. 75: 167-188. K a r n a k ~ K . J. 1986. Structure and function , of the chloride cell of Fundulus heteroclitus a n d other teleosts. Am. Zool. 26: 209-224. Kresja, R. J., D. Bringas Jr., and H . C. Slavkin. 1990. A neontological interpretation of conodont elements based o n agnathan cyclostome tooth structure, function and development. Lethaia 19: 279-291. Mallatt, J. 1985. Reconstructing the life cycle

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and the feeding of ancestral vertebrates. Pages 59-68 in R. E. Foreman, A. Gorbman, J. M. Dodd, and R. Olsson, eds. Evolutionary Biology of Primitive Fishes. Plenum, New York. Mallatt, J., D. M. Conley, and R. L. Ridgway. 1987. Why do hagfish have gill "chloride" cells when they need not regulate plasma NaCl concentration? Can.]. Zool. 65: 1956-1965. Mclnerney, J. E. 1974. Renal sodium reabsorption in the hagfish, Eptatretus stoutii. Comp. Biochem. Physiol. 49A: 273-280. Moss, M. L. 1968. The origin of vertebrate calcified tissues.NobelSymp. 4: 359-371. Moy-Thomas, J. A., and R. S. Miles. 1971. Paleozoic Fishes. W. B. Saunders, Philadelphia, Pennsylvania. Nancollas, G. H., and B. Tomazik. 1974. Growth of calcium phosphate on hydroxyapatite crystals: effect of supersaturation and ionic medium. J. Phys. Chem. 78: 2218-2225. Northcutt, R. G., and C. Gans. 1983. The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. Q. Rev. Biol. 58: 1-28. Pang, P. K. T., R. W. Griffith, and J. W. Atz. 1977. Osmoregulation in elasmobranchs. Am. Zool. 17: 365-377. Potts, W. T. W., and G. Parry. 1963. Osmotic and Ionic Regulation in Animals. Pergamon, New York. Repetski, J. E. 1978. A fish from the upper Cambrian of North America. Science 200: 529-531. Riegel, J. A. 1986. Hydrostatic pressures in glomeruli and renal vasculature of the hagfish, Eptatretus stoutii. J. Exp. Biol. 123: 359-371. Robertson, J. D. 1957. The habitat of the earliest vertebrates. Biol. Rev. Cambr. Philos. Soc. 32: 156-187. Romer, A. S., and B. H. Grove. 1935. Environment of the early vertebrates. Am. Midl. Nut. 16: 805-856. Sansom, I. J., M. P. Smith, H. A. Armstrong, and M. M. Smith. 1992. Presence of the earliest vertebrate hard tissues in conodonts. Science 256: 1308-131 1. Smith, H. W. 1930. The absorption and excretion of water and salts by marine teleosts. Am. J. Physiol. 93: 480-505. . 1932. Water regulation and its evolution in fishes. Q. Rev. Biol. 7: 1-26. Spjeldanaes, N. 1979. The paleoecology of the Ordovician Harding sandstone. Palaeogeogr. Palaeoclimatol. Palaeoecol. 26: 317-347. Teeter, J. 1980. Pheromone communication in sea lamprey (Petromyzon marinus): implications for population management. Can. J. Fish. Aquat. Sci. 37: 2123-2132. Withers, P. C. 1992. Comparative Animal Physiology. Saunders, Fort Worth, TX. Yu, J. Y.-L., W. W. Dickhoff, P. Swanson, and A. Gorbman. 1981. Vitellogenesis and its hormonal regulation in the Pacific hagfish, Eptatretus stouti. Gen. Comp. Endocrinol. 43: 492-503.

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References cited
The Early Vertebrate Astraspis, Habitat Based on a Lithologic Association David G. Darby Journal of Paleontology, Vol. 56, No. 5. (Sep., 1982), pp. 1187-1196.
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The Genesis of Neural Crest and Epidermal Placodes: A Reinterpretation of Vertebrate Origins R. Glenn Northcutt; Carl Gans The Quarterly Review of Biology, Vol. 58, No. 1. (Mar., 1983), pp. 1-28.
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A Fish from the Upper Cambrian of North America John E. Repetski Science, New Series, Vol. 200, No. 4341. (May 5, 1978), pp. 529-531.
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Environment of the Early Vertebrates Alfred S. Romer; Brandon H. Grove American Midland Naturalist, Vol. 16, No. 6. (Nov., 1935), pp. 805-856.
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Presence of the Earliest Vertebrate Hard Tissues in Conodonts I. J. Sansom; M. P. Smith; H. A. Armstrong; M. M. Smith Science, New Series, Vol. 256, No. 5061. (May 29, 1992), pp. 1308-1311.
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Water Regulation and Its Evolution in the Fishes Homer W. Smith The Quarterly Review of Biology, Vol. 7, No. 1. (Mar., 1932), pp. 1-26.
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