Provocari Evolutionare Ale Mediilor Extreme

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326 T.H. WATERMANJOURNAL OF EXPERIMENTAL ZOOLOGY (MOL DEV EVOL) 285:326359 (1999)

1999 WILEY-LISS, INC.

The Evolutionary Challenges of Extreme

Environments (Part 1)TALBOT H. WATERMAN*Department of Molecular, Cellular and Developmental Biology, YaleUniversity, New Haven, Connecticut, 06520-8193

*Correspondence to: Talbot H. Waterman, Emeritus, Departmentof Molecular, Cellular and Developmental Biology, 802 KBT, Yale Uni-versity, PO Box 208203, New Haven, CT 06520-8193.

Received 3 March 1999; Accepted 9 September 1999

Extreme environments, such as the polar re-gions, clearly engage a wide range of animals eventhough these major sectors of planet earth presentconditions that not only limit animals survivaland reproduction but also may even block themaltogether. Yet the remarkable faunas pushing the

frontiers in all corners of the earth imply that ex-treme environments are not evolutionary deadends. Instead, they offer the supreme challengeto lifes capacity to adapt, by whatever means itcan, to far-from-average conditions. Evolving tolive in extreme environments relates not only tothe origin and extinction of life but also providesparticular insight into lifes inherent capacitiesand limitations in the many habitats potentiallyavailable on earth and elsewhere in the universe.1

Although animals are no match for numerousmicroorganisms in this regard, many animals dothrive under conditions hostile to most eukary-

otic life (Hand and Hardewig, 96). The major geo-graphic frontiers for animals lie in a number ofextreme habitats such as deserts and the deepseas. There physical and chemical features andshortage of food provide the major challenges toanimals well-being and fitness. In such ecosys-tems, the quantity and variety of life at all levelsis severely challenged and typically much reduced.

If stressful conditions, such as food or watershortages, increase over time or with geographiclocation, the numbers and diversity of residentanimals decrease until only a few species or evena few individuals of one species have the right

physiological or other attributes to maintain them-

selves. For instance, a large deep lake at 81 de-grees north in the high Canadian Arctic containsonly one fish species, a nonmigratory populationof arctic charr (Babaluk et al., 97). Accordingly,extreme environments typically have less complexbiological stresses than habitats less restrictive

in their physical and chemical aspects. In re-source-rich environments, the food web usuallyincludes predators on plant eaters, predators ofthose predators, and so on to top predators suchas eagles and tigers.

Yet, each step in such a sequence adds a majorloss, perhaps tenfold, of overall efficiency in thebiological use of the suns energy. As a result thefrontiers, usually being energy-poor, rarely sup-port luxuriant food webs with many levels. Thus,extreme habitats tend to have simplified foodwebs, as well as less competition, less predation,and fewer parasites (but see Cloudsley-Thompson,

96) Beyond certain limits, even the hardiest can-not persist, as in parts of the sand dune desert ofthe Arabian Peninsulas Empty Quarter or thecentral area of Greenlands ice cap. Then one ormore stresses exceed the last survivors limits.Death and extinction follow.

Probably this restraint on animals in extremeenvironments depends on the low level of primaryproductivity in nearly all such habitats. Any com-petition for this scarce resource compounds thestress. Active animals living anywhere must haveenergy food as fuel for their metabolic machine.If this resource becomes limited, so does energy

for survival, growth, and reproduction as well asfor further adaptive changes (Parsons, 94). As aresult, in order for a livable environment to sus-tain a fauna, it must have ample photosynthesis,microbial chemosynthesis, or some means of ac-

1This essay is a more technical and detailed version of the lastchapter of the authors book about extremophile animals, AnimalFrontiers, to be published by the Yale University Press. Some addi-tional material has been drawn from earlier chapters to make thisessay more self-sufficient. This part 1 of three focuses on currentlyproductive ways to study the evolution of animals living on the ex-treme frontiers. Part 2 will concentrate on long-term evolutionarytrends and their relation to natural selection and the environment.Part 3 will discuss sources of phenotypic variation, rates of evolutionextinction as a component of evolution, and extremophiles future.


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EVOLUTIONARY CHALLENGES OF EXTREME ENVIRONMENTS (1) 327

quiring food produced elsewhere (Marshall, 96).In the absence of preexisting edible organisms,environments that lack all three possible new foodsources, exclude animals except for transient vis-its. A compromise may be made by adaptive re-sponses that accommodate periodic starvation.

Also the need for energy may be postponed inmost major animal types, both vertebrate and in-vertebrate. This is possible because prolonged lackof food, and other stresses, evokes a major reduc-tion in metabolism (Hand and Hardewig, 96). Thatshutdown may be brief or may last for years in somesort of dormancy, torpor, estivation or hibernation(Pedler et al., 96). This only works temporarily, how-ever; active survival requires an end to such dor-mancy before internal resources are exhausted.

Even at the extremes, basic animal diversitywith its inherent bounty usually includes a few

tough or flexible types that can make out. Suchfrontier species, such as polar bears and wilddromedary camels, somehow flourish despite oneor more stresses, such as extreme high or low tem-peratures, high salinities, low or temporarily ab-sent oxygen, crushingly high pressures and otherinsults to the easy life. Meanwhile most others,including quite closely related species, die of ad-versity. Even the most hardy animals may freeze,be cooked, dry out or starve to death if stressedbeyond their ultimate limits.

Perspective on these matters may be providedby recalling the relativity of stressful and ex-

treme (Bijlsma and Loeschcke, 97). As used here,a stressis any factor that hinders the normal well-being of an animal, its growth, and/or its rate ofreproduction. For example, the supersaturatedsalinity of Great Salt Lake in Utah is so stressfulfor most aquatic animals that it is rapidly lethal.However, the brine shrimpArtemiareadily copeswith the high salinity and thrives there normallywithout evident stress.

Similarly the near lifeless, vast surface ex-panse of the floating Arctic ice sheet is practi-cally the obligatory habitat of the polar bear,which flourishes there year-round. Yet again,

its environment is stressful to the lethal pointfor nearly all other animals. Extreme, in con-trast can be defined relative to nonbiologicalfactors, such as global averages for ground levelair temperatures and oxygen level (219 ml/li-ter), for rainfall, for seawater surface tempera-tures (about 17C) or average water salinity (35parts per 1000), acidity, alkalinity (pH at thesurface about 8.0) and oxygen content (about 6ml/liter). Extreme, but just livable, deviations

from these averages characterize the frontiersand challenge their potential inhabitants.

Organisms with extraordinary tolerance of en-vironmental stresses have been dubbedextremo-philes. The first so-called extremophiles weremicroorganisms living at temperatures near orabove 100C (Horikoshi and Grant, 98). Yet oth-ers flourish around 0C or in strongly saline, acidicor alkaline media or at 1000 atmospheres of pres-sure in the deep seas. Many in addition endurelong stressful periods as resting spores, perhapsto the extent of surviving for millennia and trans-port through outer space (Postgate, 94).

Thus both the brine shrimp and the polar bearare extremophiles. They are presumably notstressed by their normal, but extreme, habitats.

Yet if the habitat changed, or the animal were tomigrate elsewhere, they might or might not be-

come stressed depending on their range of toler-ance or capacity to adapt. If stress does result, itultimately signals the animal to respond withadaptive changes, including evolutionary ones thatmatch the new habitat more closely (Hummel etal., 97). The challenge will be met if and whenthe animal can restore its original normal physi-ology, growth, and reproduction. If that fails, thetaxon will no doubt continue to lose fitness andbecome a candidate, official or not, for the endan-gered species list

OBJECTIVES

The goal of this essay is to inquire how so manyspecies have managed to evolve and live actively,dangerously close to the brink of death or extinc-tion. Chance and change at many levels constantlyrealign extremophiles tolerance to stress. How-ever, extreme habitats may be considered by someto be marginal and hence rather unimportant.

Also, major highly stressful environments tend tobe practically inaccessible and nearly impossiblefor biological field research. Despite this, the deepsea, polar regions, and the worlds deserts togethercover nearly three-quarters of the earths surface.The Andean altiplano and the Tibetan plateau

plus all the worlds high mountains add a non-trivial fourth ecosystem to the other three. Per-haps the deep sea occupies 65% of all this space.

Accordingly, extreme environments, far from be-ing marginal, make up a major and rather ne-glected part of our planets total space (Bailey, 98):

Land areas with a marked deficit of watercomprise the largest terrestrial climatic re-gion of the globe covering about a third or


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328 T.H. WATERMAN

more of its land surface (Arritt, 93). Perhapshalf of this total qualifies as desert, whilemore than 10% consists of extremelydry re-gions without measurable precipitation for ayear or more. Very aridareas add up globallyto far more than the area of the whole UnitedStates. Deserts have in the 1980s and 1990sbeen growing significantly both in area andin the numbers of their human inhabitants.Besides their defining water shortage, desertspresent searing heat (and in some cases incentral Eurasia, freezing cold), as well asscarce food, including self-defending thorny,tough, and sometimes toxic plants (Tollrianand Harvell, 99).

The south polar continent, as judged by thearea of its ice cap is nearly twice the size of

Australia and lies astride the South Pole

(Fogg, 98). Only about 3% of Antarctica is notpermanently covered with ice and snow to anaverage depth of 1900 m, with the maximummeasured well over 4000 m. In contrast tothe southern polar continent, the Arctic Oceancovers a large enclosed north polar area fivetimes that of the Mediterranean. The deepcentral part of the Arctic Ocean (4300 m deepat the pole) is perennially covered with float-ing sea ice and snow 23 m thick. Polarstresses on land include temperatures far be-low 0C, strong winds and storms, up to 6months of no direct sunlight, permafrost

(making underground burrows and other suchshelter impossible) and minimal primary pro-ductivity. Polar marine environments, in con-trast, are much less extreme. Except forseasonal ice shelves, they have year-roundtemperatures above seawaters freezing point,and around Antarctica have high summerproductivity. During the Arctic summer, pro-ductivity is severely limited by floating per-manent ice and snow, strongly reducing thesunlight available for photosynthesis in theice and the water under it.

Highaltitudes may be defined to lie between

4000 m and 6000 m, which in some globalareas marks the elevations between the treeline and the permanent snow line (Chapinand Krner, 95). Above that snow line smallor microscopic animals predominate, includ-ing springtails, mites, midges, and moths,mostly living in or near the surface soil. Ex-tremehigh altitudes could refer to elevationsbetween 6000 m and 7000 m, which includesthe limits of the highest land animals, such

as a few spiders and insects. Only in centralAsia, particularly in the Himalaya, are theremountain peaks over 7000 m. The highest al-pine region extends up to 8840 m, the high-est land elevation on the planet. At evengreater altitudes certain flying and windborneanimals may still spend part of their lives.Depending on locations, low temperatures,high UV radiation, precipitous terrain, gla-ciers and permanent snow, shortage of liquidwater, and low primary productivity are highaltitude stresses for animals. The low partialpressure of oxygen is also critical at least formammals and birds.

The deep sea is the largest habitat on earthboth geographically and in terms of its enor-mous livable volume. Seawater averagingnearly 3800 m in depth covers 70% of the whole

world. The deep sea may be defined as extend-ing from its beginnings beyond the margins ofthe continents, say at 200 to 300 m depth, allthe way down to the bottom of the deepesttrenches at nearly 11,000 m (Gage and Tyler,91). Deep-sea stresses include lack of photo-synthesis, cold temperatures 2C to 3C abovezero, permanent lack of all sunlight below 800m to 1200 m depth and increasing hydrostaticpressures with depth up to 1000 atmospheresin the deepest trench. Note that the quite spe-cial biological environment of internal parasiteshas not been included for emphasis here even

though the hosts efforts at rejection may behighly stressful.

Animal frontiers are usually considered as cur-rent events. Here we address the question of howanimals present day occurrence on the frontiersmost likely came about, and thereby aim to shedlight on some of the many unanswered questionsabout their evolution. The available fossil recordof extreme environments seems scant andwidely scattered. In addition, present day ani-mal extremophiles occur taxonomically here andthere in most of the major phyla but in quite

incoherent patterns, not only in phylogeneticterms but also among the four extreme ecosys-tems highlighted here. For example, little coher-ence could be expected between the faunas of thedeep sea and deserts. The wide-ranging dataneeded for effective study extends from evolution-ary history to systematics, and to physiology andbehavior where these are known at all. To avoidbecoming bogged down in isolated clusters of de-tails, current knowledge of extremophile evolution


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has been organized here by including it as part ofa more general discussion of current conceptsbroadly relevant to evolution.

This three-part essay begins with current opin-ions about lifes origins and subsequent animalphylogeny plus several overall trends involved. Itcontinues by arguing for continued broadening ofthe base of evolutionary studies by more vigor-ously including, among other things, developmen-tal and ecological insights. Some limitations ofrecently ascendant molecular genetics as a self-sufficient discipline are becoming obvious (Cum-mings et al., 99; Doolittle, 99). This discussionthen continues by considering the key roles ofnatural selection and phenotypic diversity. Therole of extinction in evolution and some thoughtson evolutions future conclude the essay.

LIFES BEGINNINGS

Since life began perhaps three or four billionyears ago, the earths geography and climates havevaried enormously (Lunine, 99). Obviously for ani-mals survival, the earths geological history andanimals ways of life have somehow to remain suf-ficiently well correlated. Evolution needs to be un-derstood not only as history but also as aprocesslargely involving animals responses to new orchanging environments. Extremophiles obviouslymust either represent the earliest type of organ-ism or they must have evolved from less hardyand more average founders, as some biologists be-

lieve. In either case, the originof life and, muchlater in time, the origin of many-celled animals,as well as their ensuing global evolution, involvecrossing particular frontiers for the first time.

In a way, the origin of life (and its innumerablekinds of living things) is rather like an ecologicalfrontier with its polarity reversed. In deserts oron high mountain peaks, animals are constantlypushing out from known livable territory to ex-pand their limits into the unknown. If they ex-ceed their ultimate limits, they die and becomeextinct. At its origin, on the other hand, life iscrossing the frontiers inward from non-life to life.

This remarkable transition requires moving froma habitat incompatible with life to one where lifeis just barely possible.

At the beginning of time, conditions in the uni-verse were not remotely compatible for life to sur-vive even momentarily. Many things had tohappen and billions of years pass before our moteof a planet was formed, cooled, and gradually be-came able to sustain life. Not surprisingly, the ori-gin of life has long been a matter of intense

scientific interest and debate (Pace, 91). Like itstiming, lifes original components and its venuealso remain quite uncertain. Enzymatic and self-replicating molecules were necessary for life tobegin as well as to provide energy for metabolism.

Obviously the question of where lifes essentialraw materials came from is critical. Substantialamounts of simple organic compounds occurwidely in interstellar space. Presumably the sunsultraviolet rays formed these from inorganic pre-cursors, such as ammonia, methane, carbon diox-ide, and water (Schidlowski and Aharon, 88).Carbonaceous material, somewhat like humus insoil, is common in some meteorites, snowball-likecomets, and other extraterrestrial bodies (Croninand Pizarello, 97). The occurrence of lifes rawmaterials so widespread in the cosmos suggeststhat life might well have arisen at any site that

presented the right environment (Parsons, 96).If so, life could have originated in more thanone place in the universe and repeatedly (Dick,98). Although assuming an extraterrestrial ori-gin for life on earth may seem to beg the ques-tion, some other (unknown) celestial body mighthave presented more favorable conditions for thisevent earlier than did the earth. Once present onour planet, billions of individual organisms, whosesize, complexity and diversity have increasedmightily over time, arose from the first one-celledprokaryote having lifes special properties.

The first living cellular organism on earth prob-

ably arose from precellular nonliving starting ma-terials well over 3.5 billion years ago (Mojzsis etal., 96). Identifiable fossils of stromatolites ex-tend back to that date at a site in northwestern

Australia (Schopf, 96, 99). These apparently areremains of shallow water marine filamentouscyanobacteria. They are considered to be ad-vanced, rather than primitive, prokaryotes withoxygen-releasing photosynthesis, an internal ge-netically controlled daily clock (Ishiura et al., 98),and oxygen-requiring respiration. The notion thatlife originated in some warm shallow marine la-goon or pond, rich in the carbon compounds

needed to form an organism, was one that CharlesDarwin, in the middle of the nineteenth century,thought plausible. Many after him have thoughtso too.

Today, the warm pool as a cradle for life mayseem more likely for the origin of animalsthan itdoes for the origin of life itself (Reysanback et al.,99) (although some scientists continue to supporta mild original habitat [Galtier et al., 99]). Sug-gestive evidence for a stressful hot site for lifes


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origin may be seen in the ubiquitous ability ofmicroorganisms to synthesize various families ofheat shock proteins (Forreiter and Nover, 98).Heat stress, as well as some other stressors, acti-vates the genes concerned and the resulting chap-erones in turn help prevent or repair damage tostressed cells. Yet this early prokaryotic adaptiveshock response has been conserved in all eukary-otes including plants and animals, that seem ba-sically not to be thermophiles.

More than 3.5 billion years ago, the earth wasonly beginning, perhaps intermittently, to presentsurface conditions mild enough for the simplest,toughest life to begin (Lunine, 99). Nitrogen car-bon dioxide and water vapor, but little oxygen,were present in the atmosphere at that time. Hy-drothermal vents (discovered on the bottom oftodays deep ocean in the 1970s), volcanic activ-

ity, and locally high temperatures, perhaps atabout 70C in the ocean, were pervasive. Bom-bardment by asteroids and interplanetary debriswas less drastic than in still earlier times but con-tinued to make lifes survival chancy (Chang, 99).

In line with such likely hostile ancient condi-tions, it has been suggested that instead of inplacid mild shallow seas, lifes beginnings occurredunder conditions now mainly located on the oceanfloor at depths of 1000 m or more (Humphris etal., 95; Nisbit and Fowler, 96). There, in a vari-ety of geographic locations, including the Mid-atlantic Ridge, hotmineral-rich water today flows

out of rather transitory open vents or black smok-ers. Under the prevailing conditions of high pres-sure and high temperature plus injection into coldsurrounding water, amino acids and other mol-ecules necessary for life might spontaneously formthere from simpler precursors (Russell and Hall,97; Amend and Shock, 98; Huber and Wchters-huser, 98; Imai et al., 99). This could be an al-ternative or supplement to organic material fromouter space, already mentioned.

Some general support for lifes origin in extreme,but not necessarily deep-sea, environments, highlystressful for most present-day organisms, comes

from a major group of living microbes, theArchaea(Woese et al., 90). Many archaeans, as well asbacteria, are extremophiles of which differentkinds flourish under various conditions lethal tomost life (Atlas and Bartha, 98):

High acidities comparable to concentrated sul-furic acid

Similar extreme alkalinities Hot-spring and deep-sea vent temperatures

approaching or even exceeding the sea-levelboiling point of water

High pressures reaching 1000 atmospheres indeep-sea trenches

Extreme salinities of saturated brine Cold temperatures at or below 0C (Russell

and Hamamoto, 98)

Interestingly, the lipid cell membranes of Ar-chaea are distinctly different from the glycerol-based bilayers typical of bacteria and eukaryotes(van de Vossenberg et al., 98). The archaeanmembranes stability against various extremestresses and its low permeability to ions and pro-tons seem basic to archaeans capabilities as cham-pion extremophiles or superbugs(Davies, 98).

Such hardiness could, no doubt, have been ofsurvival value in the likely harsh early days of

lifes existence, although lack of strong evidencefor this leaves room for some doubt (Miller andLazcano, 95). In addition, some archaea, likesome bacteria, can derive their metabolic en-ergy anaerobically from inorganic compounds(Pace, 97). Yet, more than half the genes in thefirst archaeon to be fully sequenced were pre-viously unknown in any organism (Bult et al.,96). Certainly some such stress-embracing, selfsufficient organisms should typify the earliestsingle-celled marine life. Available evidence im-plies that the beginnings of life on earth didtake place in a marine medium (but see Knauth,

98), that then contained, even near the surface,only traces of oxygen.

Genetic evidence has suggested that the lowestand deepest family trees branches of the arch-aeans and bacteria are apparently occupied byhyperthermophiles flourishing at temperatures upto 100C and even to 150C at deep water pres-sures (Davies, 98). More than 50 species of suchprokaryotes are known; one of them, at least, re-produces successfully only at temperatures above90C (Stetter, 98). Accordingly, the earliest lifemay have been anaerobic, chemotrophic, hot wa-ter requiring, superbugs.

Rich assemblages of such organisms are foundtoday deep in the earths crust beneath both theland and the ocean bottom around hydrothermalvents and the spreading zones of midocean ridges.Perhaps such environments provided relativelystable, if barely livable, habitats when the globessurface was still receiving frequent massive impactsfrom interplanetary debris. However, data for theevolution of prokaryotes, largely based on riboso-mal RNAs, have become less unambiguous and


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more contentious in the late 1990s as more prokary-ote full genomes became available (Pennisi, 99)

The subsequent rich development of protists,single-celled algae, and protozoans, such as ame-bas (Sogin and Silberman, 98) was also marine,but presumably less extremophilic. Later, theextensive evolution of early multicellular plantsand animals followed. A substantial ocean hasprobably been present on earth for 34 billionyears. Yet the present day ocean floors, becauseof their ongoing origins in spreading fromworldwide midocean ridges, are mainly lessthan 100 million years old (Nicolas, 95). Pre-sumably, this would preclude the preservationof any deep-water marine fossils earlier thanlate Mesozoic. Also, the world ocean and its cru-cial current system have changed their patternsrepeatedly as continental tectal plates have

ranged from equator to poles.Deep ocean water, in addition, may have hadinadequate oxygen for animals until 1 billion to0.5 billion years ago (Canfield, 98). Such anoxicconditions would block both animal invasion of thedeep sea and the survival of any preexisting deepfauna, evolved during previous adequate oxygenconditions. The history of the oceans salinity stillseems rather controversial (Knauth, 98). Althoughprokaryotic life began more than 3.5 billion yearsago, the first many-celled animals did not appearuntil much later, probably about 1 billion yearsago. Yet long before animals arose, single-celled

eukaryotic algae (Kerr, 95) and protozoans alsoflourished in the sea as did many-celled plants(Vidal, 94). Meanwhile animals direct ancestors,presumably some single-celled eukaryotes (Sogin,97), had lost several remarkable metabolic fea-tures prominent in many microbes. For one thing,there is little or no evidence, based on their habi-tats and the nature of probable surviving relatives,that suggests the first animals were extremophiles.Instead the earliest animals apparently evolved ina moderate inshore marine environment and atrather stable liquid-water temperatures, probablyin a range of 1525C.

If these conjectures about the earliest cellularlife of microbes and the earliest many-celled ani-mals have some validity, we can conclude thattheir respective ancestral types were quite distinctin their habitat needs. The earliest prokaryotes,both bacteria and archaea, were probably by theirnature extremophiles, flourishing at temperaturesup to 85C or 95C over a broad range of acidi-ties, alkalinities, and salinities (Atlas and Bartha,98; but see Galtier et al., 99). In addition, their

metabolism did not depend on the presence of freeoxygen gas, scarce in earths early atmosphere andaquatic environments. They also could synthesizeorganic carbon compounds for their cytoplasmfrom inorganic raw materials. Hence they werenot dependent on other living organisms, whichindeed did not yet exist, as energy food.

In contrast, the earliest many-celled animalsrequired substantial oxygen to breathe, were com-parative weaklings in the face of harsh conditions,and had to obtain food by eating other organismsor absorbing organic molecules originally synthe-sized mainly by photosynthesis or to some extentby chemosynthesis in certain prokaryotes. To func-tion in the worlds extreme environments, animalsmust have had or developed a strong capacity toevolve adaptively. Probably unlike the earliestprokaryotes, animals had to redevelop resistance,

stability, and hardiness to extreme temperatures(Johnston and Bennet, 96) and other potentialstresses of many sorts. They need such capacitiesto thrive in the extreme environments, variouskinds of which were surely widely present on earthfrom very ancient times. For instance, ecologicalevidence for glacial activity and probably a sub-stantial ice sheet in northern Canada, dates backmore than 2 billion years in rocks now in Europeand North America (Benn and Evans, 98). Laterglacial conditions were widespread during latePrecambrian and much of Paleozoic times.

Yet, the long delay between the first life on earth

and the origin of animals, seems to have dependednot on their eventual adaptation to low or no oxy-gen (which they have done only marginally up tothe present), but on a fortuitous change in theearths atmosphere and the seas. Probably the ar-chaic earths atmosphere, when life began, con-tained only a trace of oxygen along with muchcarbon dioxide. Long ago, photosynthesis waslargely responsible for the global conversion of theancient atmosphere to its recent pattern with 21%oxygen and only a trace of carbon dioxide (Fal-kowski and Raven, 97). The whole process mayhave begun as long as 3.8 billion years ago

(Schidlowski and Aharon, 88).In turn this great shift in atmospheric gases,

effected by cyanobacteria and later green plants,made way for the whole animal kingdom to ariseand flourish. Animals very existence depends criti-cally on abundant oxygen gas needed for theirmetabolism. After an initial moderate rise, asteeper significant increase in atmospheric oxy-gen occurred around 1 or 2 billion years ago(Deutsch et al., 98), just when multicellular ani-


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changes affect life on the globe. To survive, thoseanimals that remain in place despite such changesmust cope effectively with any stresses they im-pose. As long as a viable environment provides theenergy needed in food, animal populations tend toexpand with increasing speed to the full capacity oftheir habitats, according to Malthus law. The bio-logical forces involved in such expansive emigra-tions also underlie Charles Darwins argument forthe scientific reality of evolution and the origin ofspecies (Depew and Weber, 95).

If the whole world were a single stable support-ive habitat, the first (and hence, at that time, theonly) animal species to have evolved would nodoubt have reproduced to fill it, in the sense ofusing all its resources. Current evidence showsthat the family diversity of both bony fishes andtetrapods has evolved exponentially through their

history. This may imply that such a process ofgrowing to fill a global environment has not yetreached its capacity to accommodate new animaltypes (Benton, 98).

This expanding through overcrowding model, ofcourse, may seem simplistic and does not includemany factors of concern to physiologists and ecolo-gists (MacNally, 95). For instance, real environ-ments are in fact limited in area, patchy inlocation, and changeable over time. Also, the wholematter of habitat choice by animals is a complexone. Even so, simplifying to an overcrowdingmodel does seem to play out the basic scenario of

Darwinian evolution (Depew and Weber, 95). Forinstance, the morphological and genetic phylog-eny of seven closely related species of desert liz-ards suggests their progressive adaptation toincreasingly stressful arid sand dune conditions(Harris et al., 98).

However, Bradshaw (97) argues that the strik-ing hot desert success of at least a number of well-studied reptiles, such as desert lizards, deserttortoises, and some snakes, is not a result of adap-tive evolution. Instead, several physiological andbehavioral features shared by reptiles generallyare proposed to pre-adapt the class to such

deserts high temperatures, and scarcity of waterand food. Yet the importance of factors additionalto chance is surely attested by the absence ofmany reptile types and numerous species from alldeserts, as well as the quite different reptile fau-nas in various world deserts.

As in the model suggested below, speciation hereapparently was marked by a series of transfersfrom marginal to more and more severe deserthabitats, Perhaps successive speciations were fol-

lowed by displacement of the new species followedby its further adaptation to the more stressful newenvironment. Darwin himself was mainly concernedwith competition among animals as evolutions driv-ing force rather than the evolutionary consequencesof the habitat changes or differences that are ourmain concern here.

So in a more realistic world, the archetypalwarm nourishing pool in which the first kind ofanimal originated became crowded. In response,some individuals began to overflow or emigrateinto neighboring areas less favorable in tempera-ture, salinity, amount of oxygen, acidity, and soon, including the quality and quantity of avail-able food. Animals thus crowded out of paradisewould find life somewhat more stressful than be-fore. Yet because their reproduction typically resultsin considerable variation among the offspring, in-

dividual organisms generally differ in their abilityto survive under such suboptimal conditions.As a result, those able to flourish at lower or

higher temperatures, or under other potentialstresses in the new habitat, would survive leav-ing paradise. Those less fit would fail to repro-duce as well as before, or die in the new habitat.The survivors of this first emigration may be onlya small part of the original population. Yet, overtime they could also increase their fitness in thesecond habitat. In turn, they would multiply andfill up that habitat until some of their descendantswould be forced to overflow into still different, less

optimal surroundings. Eventually, of course, thefringes of such progressive expansion would reachvarious forbidding frontiers that block furtherspread.

Given unbridled reproduction, competition forfood, space, and other resources leads to the natu-ral selectionof the fittest individuals for survivalby eliminating the unfit (Bell, 97). As a result,evolutionary ecology (Brenchley and Harper, 98)is intimately related to our central topic of suc-cess or failure in extreme environments wherepush comes to shove (Hoffmann and Parsons, 97).To survive, the animal must either be already tol-

erant of the new environment or must relieve itsstress, including shortages of such essentials asdietary nitrogen (White, 93) by an adaptive re-sponses at some level.

Specifically for our present interest, we shouldnow look for the evolutionary trends that link thefirst animals to those able to flourish in extremeenvironments. How have the small simple ratherfragile earliest many-celled animals been able toevolve into the numerous and diverse extremophiles


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that populate todays frontiers? To help answer thatquestion, the total data on animal relationshipsneed to be examined for evidence for the evolutionof resilient, tough organisms or those with a strongrepertoire of adaptive responses to environmentalextremes.

One kind of tolerance that may occur in an ani-mal group depends on its previous history thathas prepared it for whatever new environmentaltrait that otherwise would have been stressful.For instance, the preferences of different verte-brates either for moist aquatic or for dry terres-trial habitats may go back eons to the origins ofamphibians, which crawled out on land as a sortof four-legged lungfish, and the later evolution ofthe first reptiles from salamander-like forms. Herestructural and functional adaptations to particu-lar habitat features have evolved over a long pe-

riod of existence under certain environmentalconditions.For instance, the striking resistance to water

scarcity and high environmental temperaturesshown by the camel may be traceable to camelidbeginnings in semiarid lands of western North

America. Conversely, in the case of some domes-ticated mammals, such as cattle, their limited ca-pacity to survive with little or no water to drinkmay be attributed to the short-term evolutionaryorigins of their ancestors in habitats where waterwas abundant. Typically, desert mammals have asignificantly smaller water flux than those living

in habitats with abundant water (Degen, 97).Similarly, human ancestors that evolved in

tropical or subtropical forests with abundant rain-fall could account for the drought intolerance oftheir present day descendants. Thus, among Aus-tralian aborigines the absence of any special physi-ological capacity to survive on scarce water couldresult from their relatively recent (evolutionarilyspeaking) entry into Australia from warm, moistSoutheast Asia. They make up for this physiologi-cal shortcoming for arid life by more rapid behav-ioral and social adaptations. These allow them tolocate the necessary water sources of their dry

habitat and organize their lives around them.In contrast, some previously intolerant animals

may somehow respond to stress by increasing theamount and range of variability on which natu-ral selection may act (as discussed below). Stressalso may increase the intensity with which selec-tion acts because diversity is lower on the fron-tiers. The few initial survivors involved in the newenvironment could increase the chances that anymajor gain in the ability to persist would increase

even though it probably would not do so in a largepopulation. Alternatively, a small marginal popula-tion may more likely become accidentally extinct.

When populations are so thin or immobile thatthe sexes would rarely meet, as in deep-sea an-gler fishes and in many parasites, availability ofmates can also become a serious problem for re-productive survival (Vollrath, 98). Among para-sites that live inside extremophiles, finding theirhosts may pose similar difficulties. For instance,deep water pelagic fishes, such as stomiids andmyctophids have significantly fewer copepod para-sites than the easier to find benthic, surface, andshallow water types (Boxshall, 98).

ANIMALS FAMILY TREE

Phylogeny and how to reconstruct it are relevantto animal frontiers for several reasons. For ex-

ample, if the first metazoans were extremophiles,the stem pioneers of the animal family tree shouldbe extremophiles. Then, most subsequent earlyand late branches and twigs of the family treewould have had to lose their tolerance and resis-tance to stress. Yet sponges, cnidarians, andprimitive flatworms, no doubt close to the firstmetazoans, do not seem to be basic frontier types.

Also, most animals are not extremophiles atpresent nor were they collectively at any time inthe past, as far as we know. If so, early and latesubsequent branches and twigs of animal phylog-eny must have independently evolved the hardi-

ness required on the frontiers, as suggestedearlier. Accordingly, our need to know where andwhen in animal evolution extremophiles evolved,once or many times, at random or in some sig-nificant patterns, makes phylogenies a key itemon our agenda. As a result, the kinds of data avail-able and the ways of using them to construct ananimal family tree need to be understood.

Many kinds of evidence provide an immensebody of information about lifes course on earthextending back 565 million to several billion yearsago (Conway Morris, 98b). Most directly, the his-torical record of evolution, as embodied in the fos-

sil and geological records, permits the globalhistory of life to be partially reconstructed, includ-ing dates and details about habitat qualities(Brenchley and Harper, 98). Despite their gapsand ambiguities (Novacek and Wheeler, 92), suchdata may provide remarkably detailed informa-tion about particular, often isolated, groups andperiods (Donovan and Paul, 98).

In addition to the direct fossil and geologicaldata, the traditional anatomical (Nielsen, 95), and


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the systematic data of animal classification (e.g.,McKenna and Bell, 97), as well as comparativedata of many kinds, are also critically helpful inreconstructing animal history (Martins andHansen, 96). Any of the major aspects of biology,including those for which only contemporary dataare available, can be used to test and, if used care-fully, to extend and strengthen conclusions drawnfrom the basic fossil and geological record (Knoll,92). For instance, morphology (Nielsen, 98), finestructure, isozymes, physiology, behavior, devel-opment, life histories, reproduction, ecology andmolecular biology are all potentially importantsources of phylogenetic inference (Littlewood etal., 98).

Even so, the use of indirect evidence in draw-ing evolutionary conclusions needs to be firmlygrounded on understanding its reliability and rel-

evance. For example, untested assumptions ofoptimality and adaptation have brought ridiculefrom colleagues and some embarrassment to com-parative physiologists on this count (Bennett, 97;Mangum and Hochachka, 98). On the other hand,little attention has been paid to adaptation in thestudy of population genetics because R.A. Fishersinfluential theory discounted it and had been tac-itly accepted as gospel until recently. Adaptationas a measure of the fit between an organism andits environment is a basic biological concept (seepart 2). Adaptation, as a process, is a complex mul-tilevel response of the organism to change (Slobod-

kin and Rapaport, 74).At the evolutionary level it is particularly dif-

ficult to study, not least because quantitativecomparisons between related animals may becompromised since the usual tests for statisti-cal significance are only valid for independentobservations (Felsenstein, 85). Given the greatmasses of data potentially relevant to evolution,a phylogenetic tree offers a graphic way to or-ganize and analyze particular sections or thewhole overview of animal history (Avise et al.,94). Because the first organisms reproducedand their offspring did so, in turn, for many

thousands of evolving generations, the whole oflife might be considered to be one extended fam-ilydescended from a single ancestor (Kenrick andCrane, 97). This is a huge and complex topic.

Yet, the full course of animal life, from its be-ginning to the present, can itself be modeled by ashrub-like or tree-like two-dimensional diagram,in so far as data are available. Current anatomi-cal (Nielsen, 95) and molecular (Mller, 98) evi-dence implies that all many-celled animals,

including the simple, quite offbeat sponges, seemto have originated from a single ancestor. Thatancestor was the ultimate source of all 1.5 mil-lion or so named living animal species, plus un-counted extinct and present day unknown species.

Before dealing with unresolved problems of con-structing animals historical phylogeny, the gen-eral nature of such a family tree and whereextremophiles seem likely to fit in should be in-troduced The animal kingdom splits off from theeukaryote main stem of an inclusive tree of lifeat about the same time that the fungi and thegreen plants evolved (Philippe and Adoutte, 96;but see Bonner, 98; Veuthey and Bittar, 98). Fromits original single animal stem, 30 to 35 majorbranches represent the known phyla. Some moreinclusive groupings may intervene between theoriginal stem and the phylum branchings because

certain phyla share important common featuresand have been variously placed together on oneof several early large branches, mainly on the ba-sis of:

Early development pattern Bilateral or radial symmetry Presence of two (the diploblasts) or three (the

triploblasts) body tissue layers Absence or presence and kind of an internal

body cavity (Nielsen, 95)

A large number of grouping of animal phyla,

such as protostomes and deuterostomes, havebeen proposed (Nielsen, 95; Jenner and Schram,99). However, none of the phyla, or groups ofphyla, such as deuterostomes, are evidently madeup exclusively or even largely of extremophiles (ex-cluding several minor parasitic phyla). Yet eachphylum, in turn, typically branches successivelyinto a hierarchy of classes, orders, families, gen-era, and species (the evolution of diversity will bediscussed in Part 2 of this essay). At the level ofclasses, too, there are none that are exclusivelyor largely frontier types. However, at the branchlevels of orders and families, there are undoubt-

edly many animal groups that have become ex-clusively or mainly extremophiles in our fourmajor categories.

DESERT ANIMALS

The groups of animals prominent on the fron-tiers demonstrate the evolutionary branches in-volving extremophiles. To begin with, the worldsdeserts form singular habitats in the sense thattheir faunas and floras as well as their climate


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Andes and cold arid parts of Patagonia. The con-temporary dromedary, now mainly domesticatedor escaped from domestication, has a quite re-markable set of features that allow it to be anextreme desertophile (Wilson, 89).

Some species clusters in deserts also imply sub-stantial small-scale evolution on this frontier. Forexample, the Namibian Desert fauna includes theworlds largest assemblage of tenebrionid beetles,which number almost 200 species there. A vari-ety of structural and functional features as wellas remarkable behavioral patterns are correlatedwith these insects high fitness to Namibian con-ditions (Smme, 95). When desert stresses elimi-nate some other less hardy desertophiles, beetlesin this family may even diversify further. Remem-ber, however, that the Order Coleoptera containsabout 300,000 species. As a group then, on the

frontiers or not, successful speciation seems to betheir mtier.The Australian deserts are also special in shel-

tering numerous species of lizard (James, 94) aswell as unique marsupial mammals: kangaroos,wallabies, bilbies, bandicoots, and others notfound elsewhere. Both the Australian and Saharadeserts became severely arid relatively recently,geologically speaking, As a result, their desert fau-nas must have evolved quite rapidly from less ex-treme ecosystems. Such blooming of a particularkind of animal may depend on historical circum-stances (the marsupial explosion in Australia) and

on the way an animals basic nature happens tofit the habitat (the burst of Australian lizard spe-cies). In the case of the lizards, they share thegeneral feature of ectotherms of having metabolicrates much lower then birds and mammals. Hencemore modest energy food requirements, below av-erage water needs and heat production all sup-port their desert fitness (Nagy et al., 91).

POLAR AND DEEP-SEA FRONTIERS

Terrestrial animals at extreme high latitudesand altitudes as well as in the most stressful ar-eas of desert tend to be small soil-living insects

such as collembola and mites or spiders. No doubtthis testifies to their inherent high tolerance ofscarce food and extreme temperatures. Highmountains ecologically are somewhat like islandswith unusually endemic faunas dependent on themountains location, mid-continental or coastal,high or low latitudes. From an evolutionary pointof view mountains offer relatively easy access torepeated animal invasions from the surroundinglowlands and except at high latitudes, they afford

rather short range migrations from extreme tomoderate or even tropical habitats.

Long range migration has been an importantevolutionary feature for high latitudes, where themidnight sun enables summer primary produc-tivity to reach exceptionally high levels(Waterman, 88), In the Arctic both terrestrial andsubarctic marine environments are involved. Inthe Antarctic the productivity is almost entirelymarine, except for microbes (Wynn-Williams, 96)

Although birds, whales, and other marine mam-mals have been most involved in the evolution ofthis long-range annual movement, some ungu-lates, such as musk oxen (Ct et al., 97) andreindeer in the north, carry out moderate rangeseasonal migrations to feed and avoid the mostsevere terrestrial winter conditions. Clearly birdevolution at high latitudes, particularly that of

penguins, auks, and albatrosses has been moldedby the highly stressful climate combined with richnearby marine feeding areas (Bevan et al., 98).

Among the evolutionary puzzles of the Antarc-tic, one of the most interesting relates to the ma-rine bony fishes around the south polar continent.The total number of fish species known there isonly about half the number native to the North

Atlantic or to the Bering Sea in high northernlatitudes. Yet the antarctic fish species are doublethe number reported for local seas within the Arc-tic Ocean. In any case, antarctic fishes have drawnan unusual amount of scientific attention (Mac-

donald et al., 87). For one reason, those best stud-ied belong mainly to a single diversified group,the perch-like notothenioids, hardly familiar else-where. Of the more than 150 to 200 total speciesof antarctic coastal and bottom fishes more thanhalf are limited to the cluster of families in theSuborder Notothenioidea (Gon and Heemstra, 90).Notothenioids are known in other parts of theworld but are not prominent except around Ant-arctica.

Somehow the notothenioids seem to have a spe-cial license to flourish in antarctic coastal water.How this curious situation came about is still not

clear (Ritchie et al., 97). It is reminiscent of theremarkable radiation marsupial mammals under-went in Australia after that continent broke freeof Gondwana, the paleozoic supercontinent. Thereare quite a few antarctic fish fossils known fromboth freshwater and marine habitats dating backto Gondwana (Eastman, 91). Yet they seem quiteunrelated to the present exclusively marine faunathat evolved perhaps only 50 million years ago.Fossilnotothenioids have yet to be discovered.


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338 T.H. WATERMAN

In appearance notothenioids range from mainlysmall to moderate sized sculpin-like to blenny-likeor cod-like fish. Most, but not all (Eastman, 97),are bottom-living species, rather weak sluggishswimmers, and perhaps sit-and-wait predators.They are remarkable for several reasons (East-man, 90). They lack swim bladders, for one thing.For another, a striking feature of notothenioids istheir ability to avoid internal freezing at Antarc-tic seawater temperatures that are perenniallybelow teleost bloods regular freezing point.

This capacity depends on the year-round syn-thesis of antifreezes glycoproteins by the fishsliver (DeVries, 83). Arctic cod have independentlyevolved antifreeze glycoprotiens closely similar tothose of antarctic notothenioids (Chen et al., 97).Quite often other moderately high latitude fish,such as flounder, produce blood antifreezes but

only seasonally. The compounds involved in vari-ous cases significantly lower the temperature atwhich ice crystals form within the blood and otherbody fluids. Typically, the molecules consist ofchains of amino acid trios to which a sugar is at-tached (Whrmann, 95). The various antifreezemolecules have a wide range of molecular weights.

Notothenioids also are unique among verte-brates in having one family, the Channichthyidae,with 18 species, whose adults completely lackblood hemoglobin and have only traces of, or no,muscle hemoglobin. As a result, the blood of theso-called ice fish can carry only about 10% of the

oxygen held by their red-blooded relatives. Thiscould limit the scope of the fishs swimming ac-tivity and its ability to withstand low levels ofenvironmental oxygen. But antarctic coastal wa-ters are generally saturated with oxygen, andnear-freezing seawater contains about 60% moreoxygen than it would at 20C. Yet as if to com-pensate for its bloods low oxygen capacity, the icefish heart is two or three times larger relativelythan is usual in bony fish (Feller and Gerday, 97).The amount of blood pumped per beat in ice fishis also many times the typical volume (Tota, 97).In addition, their total blood volumes are several

times those of relatives with normal blood hemo-globin (Acierno et al., 95).

Furthermore, channichthyids depend more thantypical bony fishes on oxygen uptake through theskin. Mitochondrial densities are also markedlygreater in ice fish swimming muscle. On the otherhand, the hemoglobin-free blood may be an ac-commodation to low temperatures since the bloodviscosity of ice fish lacking hemoglobin is abouthalf that of notothenioids with normal red blood.

Decreasedblood viscosity would reduce the pump-ing work required of the heart and thereby mightcounteract the increasein blood viscosity causedby lower temperatures.

Another of the many other fish groups presenton the antarctic sea floor is also represented by aburst of species. These are the so-called snailfishes, which make up the family Liparidae. Theseare reasonably common as museum specimensfrom worldwide abyssal deep seas but are other-wise little known. Like many benthic fishes fromgreat depths, these have strangely large heads andsmall tapering bodies (Gage and Tyler, 91).Liparids are common in antarctic deep water andwhen properly studied systematically, with spe-cies numbers probably reaching 50 to 60, may ri-val notothenioids (Eastman et al., 94). Myriadother types of bony fishes, common elsewhere, are

not found at all in the Southern Ocean.In view of the weak or no daylight, low tem-peratures just above 0C, high pressure and lownutrition stresses in deep water, the presence ofmany types and species of animals there, rangingfrom single-celled protozoans to whales all the wayto the deepest ocean bottoms, seems remarkable.In addition, despite the stresses, certain evolu-tionary immigrants into the depths, such as lan-tern fish (myctophids), grenadier fish, amphipodcrustaceans, and sea cucumbers, have evolvedmany species on the deep-sea frontier. The geo-logical history of the oceans must have closely in-

fluenced such evolution in the deep sea (Van derSpoel, 83). Sea-bottom origins from midoceanrifts, continental drift, land uplift and subsidence,and changes in the oceans circulation, as well assalinity, depth and temperature must all have hadmajor effects (Kerr, 91; Grigg and Hey, 92).

The bony fishes of the deep sea, by far theworlds largest extreme environment, also offer anumber of substantial evolutionary flowerings ofmany families and several orders of deep-livingextremophiles (Stiassny et al., 96). For example,two substantial and fairly early branches of theneoteleost family tree comprise some of the most

diversified, best known, and numerous pelagicdeep-sea fishes. The lantern fishes in the OrderMyctophiformes and the diverse relatives of thestomiid dragon fishes in the Order Stomiiformeslive in the twilight zone of the open sea between800 and 1200 to 1500 m where penetrating sun-light reaches its deepest depths in the clearestwater (Jerlov, 76).

Interestingly these barely-lighted (even at mid-day) depths also tend to maintain the highest di-


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versity of deep midwater animals in general, in-cluding crustaceans and squids (Clarke, 96) aswell as fishes. Remarkably, the myctophid-like andstomiid-like fishes have diversified exuberantly forlife at this depth range, far below the shallow lev-els where photosynthesis can be effectively pro-ductive (usually only in the surface 50 to 100 mor so). Hydrostatic pressures at twilight zonedepths vary from 80 to 150 atmospheres. Nearlyall of the abyssal fauna down to the deepesttrenches at 11,000 m depend for food on any down-ward sinking organisms (including phytoplankton)(Smith and Kaufmann, 99), as well as migratorsand deep divers plus the rain of plant and animaldetritus and carcasses falling down through thewater column. Whale carcasses on the deep bot-tom form ephemeral mini-ecosystems there (Feld-man et al., 98). Microorganisms are abundant

down to the deepest depths (Kato et al., 97)Returning to the mesopelagic fishes, the mycto-phids are not much modified from what may su-perficially look like small sardines or anchovies.These lantern fishes have rather small mouths,fine conical teeth, and filter-like structures ontheir gill arches that allow them to feed by swim-ming after smallplankton or nekton. Numerousboth in species and in individuals, lantern fishesworldwide are important intermediaries in thepelagic food web.

In contrast to myctophids the abundant anddiversified stomiiform fishes are deep pelagic

swimmers that pursue largeprey. Structurallythey are more modified, even bizarre, some-times with long chin barbels. Many have gap-ing mouths and long fanglike teeth. Prey threeor four times the predators length have beenfound in the stomachs of several types of suchfishes. These large prey eaters usually do notmigrate vertically on a daily cycle. Presumablyall such active deep water predators must livein particular water masses where enough foodis available to sustain some vigorous swimmingor vagabond food searches.

Both stomiiforms and myctophiforms are re-

markable for their mainly small, but opticallyelaborate, light organs (photophores) mostly on theventrolateral body surface. Like eyes in reverse,these innervated structures emit biochemicallygenerated light of controlled intensity, wavelength,and direction. This special organ system hasevolved in response to the photic challenge of thetwilight zone and occurs widely not only inmyctophids and other fishes but also in severalother deep water pelagic animals, including

shrimp-like crustaceans (mysids, sergestids, andoplophorids) and numerous squid species.

In addition, myctophids, along with many otherkinds of nekton and plankton (but generally ex-cluding the stomiiform types), may undertakedaily vertical migrations of as much as severalhundred meters extent, a major convergent be-havior pattern (Han and Straskaba, 98). Theyswim upward at dusk or before midnight, some-times to the very surface (from day depths as greatas several hundred meters) and downward aftermidnight or at dawn to 400 to 800 m or more atmidday. Closely related species may in one caseundertake such extensive vertical movements,while another apparently remains in place in deepwater day and night.

Such vertical migrations of deep-water animalsare usually explained as predator avoidance and

optimal feeding responses. During the day theysink down to less illuminated levels, where theyare camouflaged in part by light from their photo-phores and thereby made less vulnerable to visualpredators (more detail on this will be presented inpart 2). At night, protected by darkness, they for-age at shallower depths where the quantity and di-versity of food are greater than in deeper water.Below 1200 to 1500 m, permanently without sun-light, the diversity and quantity of midwater lifetapers off to a rather low level until the vicinity ofthe ocean bottom and the bottom itself are reachedat an average depth of just under 3800 m.

In another evolutionarily striking feature of thedeep-sea frontier, the bottom (benthic) fauna isquite distinct from its bathypelagic counterpart.Few, if any, myctophiform or stomiiform fishes arebenthic or even epibenthic. Instead, deep-waterbenthic and near-benthic fishes are quite remotephylogenetically from the main pelagic ones. In-deed macrourids, liparids and a number of otherfamilies of deep-water percoid fish predominateon or near the bottom. Some of these have reducedeyes or are blind. Yet, surprisingly some, such asthe macrourids and even some liparids, have largewell-developed eyes but live at depths far deeper

than any sunlight ever penetrates. Evolutionaryaspects of deep-sea vision are discussed furthernear the end of this part of the essay.

Although some may be luminescent, none of thesebathybenthic fishes have photophores like those oflantern fish and many other pelagic deep-sea fish.The phylogeny of teleosts suggests that the typicaldeep pelagic types evolved quite independently ofthe deep benthic ones. As with the beetles men-tioned above, bony fishes generally are highly di-


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340 T.H. WATERMAN

verse and species-rich, but obviously to a lesser ex-tent than insects. Teleosts, with nearly 25,000 de-scribed species, make up more than half of the45,000 or so species of vertebrates and have twiceas many species as birds and more than four timesas many species as mammals (Groombridge, 92).

Obviously, these rather intriguing scraps of in-formation and speculation about the phylogeny ofextremophiles provide a strong challenge to bi-ologists interested in such research. Much of therest of this essay deals with various current ap-proaches to evolution that may help meet thatchallenge of understanding the origins and extinc-tions of extremophiles and their potential contri-butions to insight into evolution and biology moregenerally.

PHYLOGENY PROBLEMS

Here we should return to the topic of familytrees. Although research on animal phylogeny iscurrently vigorous and varied, particularly in themolecular genetics area, many of the central ques-tions remain unanswered at a consensus level(Dietrich, 98). For instance, evidence for relation-ships between living and fossil animals is far frombeing complete and adequately evaluated. As aresult, numerous biologists, using different databases and different methods of tree construction,have produced many quite distinct and often con-tentious model phylogenies (Jenner and Schram,99; Takezaki and Gojobori, 99).

However, the similarities and differences be-tween various kinds of animals had been widelystudied long before molecular biology was discov-ered, long before Darwins time and possibly evenbefore Aristotles time. For modern use the non-evolutionary basis of the Linnean classification ofanimals (18th century) depended largely on ana-tomical comparisons and the tiered ordering ofdegrees of similarity and difference. By the middleof the 19th century, the accepted classification ofanimals turned out to be a hierarchical system ofnested categories from species to phyla and be-yond. It was, in fact, reasonably similar in its suc-

cessive levels of differences to what one mightexpect from a branching Darwinian phylogeny. Asa result, classical systematics offered a ready-made rough outline for an evolutionary geneal-ogy. Paleontologists and others took advantage ofthis and infused their geological and fossil datainto that existing framework.

Since the mid-1960s, many evolutionists haveused cladisticsto derive phylogenetic family treesby identifying successive pairs of sister groups

(Smith, 94; Nielsen, 95). Based on selected mor-phological data, this provides procedures intendedto help separate differences between similaritiesinherited directly from a common ancestor andthose resulting from parallel or convergent evolu-tion in less related lines (Raff, 96). Obviously, theclosely inherited, homologous ones are the onesrelevant to phylogeny (Abouheif et al., 97). How-ever, a level-headed approach would seem prudentin the use of cladisitcs. For one thing, the basictechnique ignores the time dimension (except forthe polarity of sequence), including independentevidence from geology or paleontology (Fox et al.,99). For another, some enthusiasts claim that cla-distics proves that birds are dinosaurs. Thereforedinosaurs are not now extinct nor ever have been(Dingus and Rowe, 98).

The importance for evolutionary reconstruction

of various secondary data sources was mentionedabove. Of all of these, molecular biology no doubthas made some of the most notable contributionsto evolution (Li, 97). The field arose after WorldWar II through the convergence of biochemistryand genetics, shepherded by a number of distin-guished physicists shifting their field of interest(Morange, 98). Basic to molecular biology is thefact that differences between individuals, species,and all the higher groups are correlated in vari-ous ways with differences in the nucleotide se-quences of their genes and in the amino acid seriesin their proteins. For some decades now the accu-

mulation of such data for DNA and RNA, as wellas many proteins, has provided a huge reservoirof relevant information in an ever increasing va-riety of animals (Hieter and Boguski, 97; Hodgkinet al., 98).

The rapidly rising tide of information, particu-larly molecular and genetic, potentially relevantto evolution has fortunately been supported by thegrowing sophistication of computers, programmingapplications, and cooperative data posting on theInternet (Hershkovitz and Leipe, 98). The newcomputational biology (Levin et al., 97) shouldbe able to carry the old theoretical and mathemati-

cal biology (Waterman and Morowitz, 65) far be-yond its earlier limitations of data handling,analysis, and applications. As a result, nuclear andmitochondrial genes and their structure, location,duplication, or loss, as well as other details of thegenetic system, have been widely used to deter-mine similarities and differences between ani-mals, closely or remotely related.

These molecular data, in addition to many otherapplications, have provided a powerful and popu-


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lar tool for amplifying the direct evidence for his-torical evolution provided by geological and fossildata (Brenchley and Harper, 98). Comparisons ofmolecular structure have, among other things, beenwidely used to confirm, extend, and directly con-struct biological family trees (Hillis et al., 96).Highly sophisticated techniques of measurementand computer analysis are extensively used to se-quence and compare the relatedness of both nucleicacids and proteins in many organisms from bacte-ria to archaea to nematodes to fruit flies to mice tohumans (Li, 97; Baxevanis and Ouellette, 98).

Analyzed in detail, these molecular data demon-strate systematic patterns of molecular variationamong animals. To use such data for constructingfamily trees, molecular biologists measure the num-bers, as well as the relationships, of sequentialamino acid or nucleotide differences between the

proteins and nucleic acids of various species, fami-lies, classes, etc. Given some important assumptionsabout how to validate and interpret the differences(Cunningham et al., 98), this approach does pro-vide a specific quantitative estimate, for instance,of animals mutational distances from one another.Thus, gene trees and molecular trees of numer-ous kinds can be constructed (Doyle, 97). Yet, thecentral biological goal is to model the actual evo-lutionary history involved, which is presumablyunique and requires knowledge of dates and rates.

Usually, reliable dating of evolution depends onavailable geological evidence, particularly for tim-

ing major branching points. Yet, in the absence ofthat evidence, if the rates of gene mutations andother changes, such as amino acid substitutions,were independently known and dependably fixed,they would provide a virtual biological clock. Ide-ally its readings could time the points of evolu-tionary divergence. But evidence increasinglyshows that changes in different molecules andgenes do occur at various rates, and these ratesmay not be constant over time or within anorganisms lifetime (Gibbs et al., 98). Obviouslyimportant for the use of molecular clocks astimekeepers (Strauss, 99) is their contested re-

liability even when recognized unreliable unitshave been discarded from the analysis. Conse-quently the responsible use of such potentiallyinaccurate clocks to date evolutionary events,particularly those in the remote past, requiresgreat care. Even so, the conclusions are almostsure to be controversial (Huelsenbeck andRannala, 97).

Although estimations of animal relationshipsand evolution from molecular data often agree

with and supplement those derived from othertypes of data (for instance, Bargelloni et al., 97),some mismatches and other sometimes seriousproblems do arise (Maley and Marshall, 98;Jenner and Schram, 99). Contradictions do occurbetween conclusions drawn from more than onekind of gene (McHugh and Halanych, 98), mol-ecule, or different species of the same group, asdo others when fossil history and the implica-tions of anatomy or biochemistry are comparedto the molecular analysis. Conclusions may alsodiffer if alternative assumptions are made abouthow to measure molecular differences and simi-larities quantitatively. Sometimes such ambi-guities threaten the phylogenetic stability oflarge data banks, such as the sole dependenceof much molecular evidence for early animalevolution on one particular structural gene, 18S

rDNA (Garey and Schmidt-Rhaesa, 98; Mc-Hugh, 98).Two kinds of problem arise from the plethora

of possible trees that have been and can be con-structed from molecular data. One is how to provewhich of these many candidates most closely re-sembles real phylogeny. The other problem is toadd a time dimension to the best phylogeny sothat it can become a true animal history. Neitherof these problems is easy to solve, and both re-main unresolved except in patchy areas of highquality. This huge enterprise remains unfinishedbecause of shortcomings in the molecular data

themselves and because the molecular biology hasyet to be adequately integrated with other rel-evant sources of data. For instance, the particu-lar species, or higher taxa, chosen for analysis mayinfluence the apparent outcome, especially formarginally small samples. Hence an adequaterange and a substantial number of relevant ani-mal types are needed to draw more than prelimi-nary conclusions about phylum and kingdomrelations (Winnepenninckx et al., 98). In addition,the particular out group chosen to root the fam-ily tree may in some cases have arbitrary majoreffects on the trees pattern (Cao et al., 98).

As a result of these and other inconsisten-cies, future research faces a substantial num-ber of problems. For one thing, random neutralmutations and molecular evolution that dependon genetic drift and are largely unconnectedwith phenotypic evolution may seem anti-Dar-winian because they discount, or bypass, natu-ral selection as a major evolutionary factor.

Also, evidence from a number of living fossilsshows that ongoinggeneticevolutionary changes


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342 T.H. WATERMAN

have occurred during the animals long historiesdespite the remarkable stasis of their generalstructure, function, and lifestyle (see discussionlater in this essay).

Similar apparent mismatches between genotypeand phenotype appear on a smaller scale, in thecommon deep-sea fish Genus Cyclothone (Miyaand Nishida, 97). Several of its 13 known spe-cies, which live at various depths between 200 and2000 m, have circumglobal populations in differ-ent oceans. These populations in a given speciesare morphologically the same. Yet maximumpairwise sequence differences in ribosomal RNAbetween populations of one such species wereshown to be about as great as the minimum dif-ference between that species and another taxo-nomic species in the same genus. How are stablephenotypes maintained in the face of evolving

genotypes?Formerly such vexing problems in evolution andthe conviction of many molecular biologists thatall matters of historical phylogeny could be de-finitively settled by studying a molecule or twofrom a few specimens of one or two living species,cast paleontology and much of biology into theshadows. Now paleontology and nonmolecular as-pects of biology are beginning to reassert them-selves (Conway Morris, 95, 98c; Mangum andHochachka, 98; Smith and Jeffrey, 98). This re-vival fortunately has been supported in geologyby major new fossil (e.g., Rougier et al., 98) and

stratigraphic discoveries as well as much betteranalytical techniques that have been developingquite frequently. Perhaps 10% of all species of tri-lobites, mollusks, echinoderms, and mammalsover time have been fossilized, and more than 60%of those may have been found by paleontologists(Paul, 98). If so, this is a better record than someestimates claim for the ratio of known-to-real to-tal species diversity in present-day tropical rainforests.

In particular, the refined use of stable isotopesin paleontology is beginning to permit remarkableinsights not only into a fossils age but also into

important basics of its environment such as sa-linity and temperature, as well as the animalsdiet and metabolism. For instance, the levels ofcarbon 12 and carbon 13 in fossil herbivore toothenamel may support conclusions about the typeof plants eaten and thus the climate of their an-cient habitat (Gillis, 96; MacFadden et al., 99).Hair, including that well preserved in humanmummies, is also important for such research(Macko et al., 99). Morphology has also been used

as evidence for reconstructing functional biologyof some fossil animals (e.g., Thomason, 95, 99).Obviously such information could be crucial foridentifying and characterizing fossil extremophileswhen they are recognized or discovered.

FIRST ANIMAL FOSSILS

Trace fossils are known in the form of tiny bur-rows about 700 million or even, contentiously, 1.1billion years old (Seilacher et al., 98). Yet, the ear-liest known actual remains of many-celled ani-mals occur in late Precambrian deposits about 600million years old (Kirschvink et al., 97). First dis-covered in Africa and later in Australia, this so-called Ediacaran fauna was later found to bewidespread on five continents (Runnegar andFedonken, 92).

A variety of quite simple flat, leaf-like, medusa-

like, sea-pen-like, or worm-like forms, all withoutshells or skeletons, occur in this primeval fauna(McMenamin, 98). Assigning them to known phyla,familiar as later fossils or as types still living to-day, is considered by some to be rather uncertain.

Yet coelenterate, segmented worm, molluskan, echi-noderm, and even arthropod relationships havebeen suggested (Waggoner, 96). Other biologists,however, consider the Ediacarans an evolutionarydead end, which did not survive the Cambrian (Bussand Seilacher, 94; Cooper and Fortey, 98). How-ever, Ediacarans have now been shown to have per-sisted into the Cambrian of South Australia (Jensen

et al., 98). In any case, there is no reason to be-lieve that these earliest animals were extrem-ophiles. Yet, geological and paleontolgical evidenceis crucial to understanding the origins and phylog-eny of animals in extreme habitats.

A major subsequent landmark in the ancienthistoryof animals occurs in the famous BurgessShale of British Columbia (Conway Morris, 98/99; Gould, 98/99). In 1909, C.D. Walcott, an

American scientist, who was then Secretary of theSmithsonian Institution in Washington, D.C., dis-covered this fauna, which had substantial shellsand skeletons. His rock quarry site in western

Canada yielded a remarkably rich assemblage ofshallow marine invertebrates quite different fromthe Ediacarans and for a time believed to date asfossils some millions of years after them (Gould,89). Important 1990s discoveries of Ediacaran-type fossils traces dating to the early Cambrianin China (Ramskold and Hou, 91), to the latestPrecambrian in South Africa (Grotzinger et al.,95) and in maritime Canada, reduced or closedthe time gap between the two faunas.


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Later search has also uncovered many addi-tional sites containing Burgess Shale-type fossilsof about the same age, located from northernGreenland to Southern Australia (Conway Mor-ris, 98a). So there is apparently a nontrivial timeoverlap of both faunas across the Precambrian-Cambrian boundary. Yet Burgess shale animals,by having exoskeletons, eyes, antennae, gills, ap-pendages, fins, and digestive tracts, seem far ad-vanced in structure from the Ediacarans, despitethis considerable overlap.

Ediacaran and especially Burgess Shale fossilsare quite astonishing. They display a remarkablywide variety of quite distinct basic types close tothe time that many, if not most, biologists con-sider marks the beginning of many-celled animallife (Erwin et al., 87). If so, this in turn suggeststhat, once such creatures got started, they diver-

sified rapidly into many distinct overall body pat-terns. A number of aspects of evolution and itsrelation to animalfrontiersare brought into fo-cus by such data, most of them in the form of un-answered questions. Why was the dawn of animallife soon marked by the appearance of so manydifferent major types? An ecosystem explosion(Waggoner, 98)?

The Ediacaran and Burgess Shale faunas wereboth highly diverse but quite different from eachother. Neither had known fossil precedent. Yetthey seem to have flourished in similar, globallywidespread, non-frontier shallow marine habitats.

Does this mean that a great evolutionary outbreakof new animal phyla occurred in shallow temper-ate or tropical seas that provided a rather uni-form, stable, animal-friendly environment? If so,what kind of drive was impelling the rapid evolu-tion of so many different body plans? This appar-ently sudden fossil appearance of many many-celledanimal types has often been called the Cambrianexplosion. Some molecular biologists and others area bit dubious about the sudden broad evolutionaryleaps implied by explosion. Even so, a number ofpaleontologists, among others, contend that it isreal and not earlier than 650 million years ago

(Conway Morris, 98b).However, as just cited, extensive molecular data

imply much earlier times for the origins of meta-zoans, protostomes, and deuterostomes, amongothers, than current geological evidence can sup-port. If such a potentially less explosive timetablewere confirmed, much of the discussion in Part 2of this essay concerning the possible mechanismsof the Cambrian explosion, could plausibly be usedinstead to explain how major evolutionary changes

were possible much earlier in time and at a lessprecipitous rate (Schopf, 98).

Among major relevant research reports pub-lished in the late 1990s, several have proposedthat these basic branchings of animals family treebegin several to many hundred millions of yearsbefore the end of the Precambrian. Several ex-amples of the applications of molecular methodsto timing important milestones, such as the ori-gin of metazoans, illustrate substantial differencesin their dates from what the geological and fossilevidence seem to indicate (Conway Morris, 98b).One of these studies used differences in aminoacid sequences in more than 50 enzymes as anevolutionary clock (Doolittle et al., 96). Accordingto that substantial protein analysis, animals splitoff from fungi and plants about 1 billion yearsago, while the earlier prokaryote-eukaryote branch

point occurred about 2 billion years ago.A second example used changes in nucleic acidsequences of seven genes for its time estimates(Wray et al., 96). That analysis pushed importantbranch points even farther back in time than didthe Doolittle et al. (96) amino acid data. Accord-ingly, chordates apparently split off from inverte-brates as long as 1 billion years ago. A third largescale analysis of brachiopods and other proto-stome groups ribosomal RNA sequences in asingle gene (Cohen et al., 98) also dates their ear-liest common ancestor deep in the Precambrianand quite long before any known relevant fossils.

Still another report carefully analyzes substan-tial base pair sequences for both a nuclear and aribosomal nucleic acid. It concludes that diver-gence of several animal phyla must have occurredmore than 680 million years ago, long before thefirst metazoan fossils known so far (Bromham etal., 98). Also, other molecular evidence that ashell-less ameboid protozoan is a foraminiferan,suggests the possibility of an extended Precam-brian evolution for this important mainly marineplanktonic group, previously known from shell fos-sils only from the beginning of the Cambrian(Pawloski et al., 99).

Despite these substantial analyses, the questionhas been raised whether available molecular tech-niques can, in fact, discriminate reliably the spe-cific branching pattern of ancient animal phylaunless the data bases were enlarged one or two or-ders of magnitude (Halanych, 98). The numerousprotostome phyla, a number of which presumablywere the earliest to evolve, seem particularly prob-lematic. Discrimination is very difficult because thepresumed rapid radiation located the branch points


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344 T.H. WATERMAN

close together and took place at least 500 millionyears ago. During that long interval a lot of mo-lecular noise has, no doubt, accumulated and atleast partly masked the original evolutionary sig-nal (Regier and Schultz, 98). How can that an-cient signal be reliably detected and read?

If validated, these various long-term molecularprojections would provide extended time for thePrecambrian divergence of phyla without an ex-plosion. Yet the estimated molecular dates con-flict strongly with the geological evidence thatmost major phyla first appeared 545 million yearsago near the late Precambrian-Cambrian bound-ary (Strauss, 99). Thus fossil evidence for originsis several hundred million years later than theprojections from molecular data. A compromisepushing the explosion back 50 million to 100 mil-lion years or more earlier than the traditional view

has been proposed a number of times (Fedonkinand Waggoner, 97; Ayala et al., 98, Conway Mor-ris, 98a; Li et al., 98). Some paleontologists arguethat these and other molecular clock extrapolationsassign points of origin far earlier than sober geo-logical evidence would permit. Although there aresome crossovers, this contrast between the pale-ontologist-geologists timing of animal origins andthat of the molecular geneticists makes it clearthat two big questions remain to be answered de-finitively. When did the various types of higheranimals first evolve on earth? Was their evolu-tion gradual and at least in part sequential or was

it one sudden multidirectional burst? The firstquestions answer remains something of a stand-off between the two camps.

The other question about whether or not manyphyla evolved nearly simultaneously involves inturn two subquestions that need to be answered.How do new distinct animal body plans, such asthose of mollusks, arthropods, or chordates, evolverapidly? What could cause perhaps 30 to 40 suchevents to occur practically at the same time? De-velopmental genetics, as discussed later, may beon the verge of explaining how new body planscan originate. But the apparent lack of a genetic

model for large scale bursting evolution, no doubt,accounts for molecular biologists lack of enthusi-asm for the Cambrian explosion.

A much more recent comparable mismatch be-tween molecular and paleontological evidence thanthat for the origin of animal phyla dates only from130 million to 65 million years ago and mammalbeginnings. Presumably this dilemma should beeasier to resolve then the much more ancient one

just discussed. Accordingly, some paleontologists

argue that molecular clock extrapolations, datingjust to the end of the Mesozoic and early Tertiary,also assign points of origin far earlier than soundgeological evidence would allow (speciation andextinction data, rates of preservation evidence,and probable lengths of missing strata) (Foote etal., 99).

For instance, Foote and his colleagues developtheir case for the origins of placental mammalsas follows: According to the geological evidence,at least nine orders or larger taxa evolved withina short period, thus comprising another evolution-ary explosion about 65 million years ago in theearly Tertiary. Yet molecular clock evidence, insharp contrast, implies a more gradual emergenceof these taxa starting about 130 million years agoin the Cretaceous. Again, according to fossil evi-dence, three new orders of insects: mayflies, cock-

roaches and grasshoppers, exploded about 300million years ago in the Upper Carboniferous (Car-penter, 92).

Although the fossil analysis appears more di-rect, the explosions it implies at high taxonomiclevels seem questionable or unexplained by cur-rent molecular genetics (Abouheif et al., 98;Regier and Schultz, 98). However, evidence hasbeen reported for explosive gene duplication dur-ing the earliest stages of metazoan evolution wellbefore the Cambrian explosion, and later, duringvertebrate evolution some time before tetrapodsappeared (Ono et al., 99).

Also phenotypic bursts or clustered origins havebeen reported at many taxon levels besides thephylum and order cases just cited. For example,as mentioned, the three multicellular kingdoms,Fungi, Plantae, and Animalia, are sometimesstated to have evolved at about the same time ina three-way branching from an ancestral stemtype. At the other extreme, speciesbursts and clus-ters among living animals, including desert anddeep-sea extremophiles mentioned previously, arenot uncommon, and some have attracted consid-erable attention. These and the related notion ofpunctuated equilibrium as a means of speciation

will be discussed in part 3 of this essay.

LARGE SCALE EVOLUTION

Whenever and whatever, the ancient historicalorigins of major phyla of animals may have been,unresolved problems about the processes involvedin large evolutionary steps remain. Some biolo-gists, for instance, believe that mechanisms thatmight initiate new phyla, classes or orders arequite different from cumulative small Darwinian-


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346 T.H. WATERMAN

Firm conclusions about specific land vertebrateorigins have yet to be reached (Ahlberg andJohanson, 98; Rasmussen et al., 98; Zardoya etal., 98). In any case this major evolutionarychange from air-breathing fish to terrestrial four-legged amphibians seems to have occurred withinabout 15 million years during the late Devonian(Carroll, 97). A variety of relevant primitive fos-sil amphibians are known (Graham, 97), and theirapparent relations suggest independent parallelor convergent evolution of key terrestrial features(Shubin, 98).

Among these early four-legged types, Acantho-stega apparently had internal fish-like gills butalso digits on its hands and feet (Carroll, 88;Lebedev, 97). Fossil fishes with skull character-istics resembling the subsequent earliest amphib-ians and several fossil amphibian types, close to

this classs fish ancestors, have been studied inthe 1990s (Ahlberg, 95). Although some frogs andtoads do well in deserts, amphibians, as theirname implies, remain semi-aquatic in their typi-cal lifestyle (Warburg, 97).

Recall that even desert toads depend on tempo-rary pools of water in which to lay their eggs andfor the development of aquatic tadpole larvae.Moist permeable skin, larval, and occasionallyadult, gills also show amphibians lingering de-pendence on an aquatic medium. Beginning withreptiles, the higher vertebrates became more fullyterrestrial in a number of ways. Reptiles, birds

and a few primitive mammals, unlike amphibians,lay eggs able to survive in quite dry air. Also theanimals skins, became less permeable and evenwaterproof.

Placental mammals, of course, retain theiryoung internally, where the mother maintainsthem in a favorable aqueous environment. Therespiratory and circulatory systems in these threehigher vertebrate groups, as well as their waterand ion regulating mechanisms and excretion,over time became increasingly adapted to terres-trial conditions (Schmidt-Niels

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