Alexander J Werth & William A Shear. American Scientist. Volume 102, Issue 6. Nov/Dec 2014.
To gaze upon a horseshoe crab is to glimpse a prehistoric Ordovician sea of nearly half a billion years ago. So moved was Charles Darwin by the appearance of these and similarly ancientlooking creatures—lungfish, lampreys, lampshells, and lycopods—that he coined the term living fossil to describe them. In his landmark 1859 treatise On the Origin of Species, he wrote that such apparently primitive species are “remnants of a once preponderant order … which, like fossils, connect to a certain extent orders now widely separated in the natural scale.” These “anomalous forms,” he wrote, nonetheless “have endured to the present day.”
Like modem biologists, Darwin was struck by the unusually archaic form of the three widely scattered lungfishes (Protopterus, Neoceratodus, and Lepidosiren of Africa, Australia, and South America, respectively), whose large lungs; cartilaginous notochord; and fleshy, lobed fins resemble those of creatures known only from the fossil record. Similarly, the coelacanth (Latimeria), another lobe-finned fish, was well known from fossils but thought to have gone extinct in the Late Cretaceous until the discovery of living Latimeria in 1938. Likewise, the dawn redwood tree, Metasequoia, was known only from fossils (10 to 100 million years old) before it was found alive in a remote Chinese valley in 1943; today it is a common ornamental that grows readily in temperate regions.
Living fossil is a perfectly appropriate and evocative term for such extant forms even today. It conveys the jarring surprise that such species conjure by retaining anatomical structures out of deep geologic time. This curious phenomenon raises evolutionary and ecological questions at once simple and profound, such as why these taxa appear to have persisted unchanged for so long, and how we can distinguish species over long stretches of Earth history without gene pools or other reproductive features essential to our current comprehension of spéciation. No doubt living fossils offer, as Darwin anticipated, an unprecedented opportunity to study-with fascinating, attention-grabbing narrativesmajor questions concerning extinction, competition, and rates of evolutionary change, both morphological and genetic. They also reveal important and often intractable difficulties of understanding the concept of species over vast periods of time.
What Is a Living Fossil?
The term living fossil itself, despite the seductive appeal inherent in its apt descriptiveness, poses challenges for the scientist and layperson alike. But even if this ambiguous term is not easily or universally defined, it nonetheless retains heuristic value. One of the chief characteristics of living fossils is an ancient or archaic form, at least externally evident, apparently retained from longlost eras. This morphological conservatism, readily seen in horseshoe crabs and coelacanths, is made all the more remarkable by our knowledge of strikingly similar fossil forms from ancient geologic ages. Living fossils are representatives of otherwise extinct groups, often common in the fossil record. Some were thought to be extinct. Nonetheless, a known fossil connection or “twin” is not necessary for living fossil status. The eel species Protoanguilla palau, discovered in 2010, is estimated to have diverged from other eels around 200 million years ago and has been described as a primitive living fossil without a known fossil record.
Much of the surprise that greeted the coelacanth’s discovery in 1938 can be ascribed to the fact that fossil coelacanthiforms were widely recognized by paleontologists, but no extant species were known. In truth there has never been any fossil find of the extant Latimeria chalumnae or L. menadoensis (West Indian Ocean and Indonesian coelacanths), undercutting the claim that Latimeria is, strictly speaking, a living fossil, and thereby deflating assertions that such species demonstrate an absence of evolution. Still, living fossil taxa tend to have only fossil (not modem) counterparts.
Unfortunately, creationists bent on denying the factual basis of evolution have increasingly misappropriated the term living fossil. In the Atlas of Creation, which pairs photographs of living fossils with similar ancient fossils, Turkish author and Islamic creationist Harun Yahya erroneously argues that “Darwinists are desperate when confronted by these fossils, for they prove that the evolution process has never existed.” Entry of “living fossil” into Internet search engines yields a preponderance of creationist websites, despite the fact that these species neither disprove nor provide any evidence counter to our understanding of evolution, which remains the cornerstone of biological science. There are no “unevolved” species, no reanimated fossils that have literally come back to life, and no living organisms that are truly identical to extinct species known in the fossil record.
What makes living fossils special, according to Harvard University evolutionary biologist Piotr Naskrecki, is simply that they superficially resemble their predecessors as members of ancient generic lines that have not been extinguished, even as they “wither through time and turn from roaring rivers of species to a trickle before disappearing altogether.” Still, they may live on in surprising ways. Naskrecki points out that our fossil fuel economy is powered by once-dominant trees of Carboniferous coal swamp forests, forerunners of the diminutive living fossil lycopod and horsetail plants underfoot today.
Conservative features alone are not enough to paint a complete picture of what constitutes a living fossil. Although Escherichia coli and other bacteria retain many traits of Earth’s first life forms (and as such are closer than most species to the universal ancestor of all living things), no one would call them living fossils, not so much due to their simplicity as their ubiquity. If living fossils were defined solely by archaic form, one could claim we are surrounded by them on land and at sea given the profusion of earthworms and jellyfish. Scarcity is thus typically a key feature: Living fossils are usually rare, with little taxonomic diversity. They may stand out, like the ginkgo tree, as exceptional organisms that are not closely related to any other living group, but which were once, according to the fossil record, common, diverse, and widespread.
None of the species generally accepted as living fossils are encompassed by a one-size-fits-all definition. Although some are rare or have narrow geographic distributions, others are common and widespread. Horseshoe crabs are found in dispersed regions and, although their populations are declining, remain abundant. As a result of their hardy resistance to pollution, ginkgo trees thrive in urban settings. Other living fossils, including the nautilus (family Nautilidae) and velvet worms (members of the phylum Onychophora), are not common but have biogeographic distributions that are fairly widespread.
Although there is often general agreement as to what constitutes a living fossil, some unusual candidates are occasionally afforded this status for a variety of reasons. A recent paper describes the pygmy right whale, Caperea, as the lone surviving cetothere, a lineage of ancient baleen whales. Other widely cited living fossil examples include a swath of organisms, from hagfishes to monkey puzzle trees (Araucaria) to fairy shrimp. Perhaps the closest thing to a true living fossil is Paleodictyon nodosum, an enigmatic creature never seen alive, known only from its deep-sea hexagonal honeycomb burrows, which are virtually identical to fossils in 50-million-year-old deposits.
Paleontological analysis of the fossil record indicates that species generally exist for an average of 500,000 to 3 million years before they go extinct or are replaced by a descendant species. This time scale poses an obvious problem for the living fossil concept, which presupposes that a species can persist unchanged for vast periods of time. Even though coelacanths and cycads appear superficially similar to species that existed hundreds of millions of years ago, they do not represent the continuation of a distinct species for such a long duration. We know that all living things keep evolving and adapting to their environments. As Naskrecki points out, living fossils are not miraculous survivors, but even if they are genetically distinct from long-lost organisms, archaic forms may carry ancient genes that might have otherwise disappeared from Earth.
Living fossil remains a problematic oxymoron, but because of its longstanding use, we can offer no better alternative. Despite its ambiguity and uneven application, we believe the term still has valuable lessons to teach in evolution, ecology, and taxonomy.
Still Changing on the Inside
One lesson from the study of living fossils is the futility of describing organisms as primitive or advanced. Despite Darwin’s admonition against use of these terms, they are based on an intuitive notion-our default view of evolution as a progressive upward path, with human beings at the pinnaclethat is hard to dispel, though it has been supplanted in modern biology by the concept of organisms as mosaics combining older, retained features with newer, specialized ones.
For example, humans share traits with other primates (stereoscopic vision, nails instead of claws), other mammals (hair, mammary glands), other vertebrates (backbone, spinal cord, teeth), and even most other animals (paired eyes and limbs, tubular gut, body cavity). On the other hand, like every species, humans have unique features: bipedal locomotion, very large brains, and reliance on symbolic language. The platypus is a classic example of a mosaic, blending ancestral features (egg-laying, poor thermoregulation) with highly derived traits, including its electroreceptive duck-like bill and venomous male spurs.
We know that various plants (including cycads, horsetails, and lycopods, and the ginkgo, dawn redwood, and Wollemi pine trees) and animals (the lamprey, sturgeon, and chambered nautilus) appear in many ways to be ancient on the outside, but their conservative external appearance need not extend to an equally archaic biochemistry or behavior. Nonetheless, the fossil record preserves external form-mainly bones, shells, exoskeletons, and other hard parts-but not other aspects of phenotype, with the exception of burrows, trackways, and other trace fossils that elucidate behavior. So it is hard to say how much (if at all) coelacanths have changed since the Devonian. Biologists know that ancient coelacanthiform fishes lived in freshwater, unlike both extant species, so in osmoand ionoregulation alone their physiology must have undergone significant changes.
In short, we must not expect that all aspects of coelacanth or horseshoe crab biology have existed unchanged for hundreds of millions of years. Alas, this dashes Darwin’s hopes that living fossil taxa might provide unsullied knowledge about the world as it existed long ago. The tuatara (Sphenodon punctatus) superficially resembles lizards but is instead the sole surviving rhynchocephalian, in contrast to squamate reptiles such as lizards and snakes. It possesses archaic skeletal and dental features and retains a median pineal eye, but has changed in many ways in the past 200 million years. Research reveals its molecular evolution is faster than that of any other known creature, so that its genetic material has changed much more rapidly than its external form. These changes provide strong evidence countering the misconception that living fossils have stopped evolving and have existed unchanged for tens of millions of years. Recent studies of molecular variation in living fossil cycads, coelacanths, and tadpole shrimp (order Notostraca) also debunk this myth.
Evolution tinkers with existing material. It does not fashion new species from whole cloth. Most major animal body plans have existed unchanged since the Cambrian explosion 530 million years ago. Sharks and scorpions, cockroaches and crocodilians all appear long ago in the fossil record, although not in their present forms. Every worm and jellyfish that evolves today is a tweaking of an ancient form, so it is impossible to say how much conservatism a species needs to be accorded living fossil status. In a real rather than metaphorical sense, all organisms hold bits of ancient life in their bodies, whether in primal enzymes or biochemical reactions, or in structures laid down according to prehistoric plans encoded by DNA sequences, which may themselves be as old as life itself, remnants of long-ago ancestors. Like all species, we humans also retain in our genome a preponderance of ancient genes dating back billions of years. Nearly 10 percent of the human genome is made of endogenous retroviruses, archaic remains of viral DNA that became integrated into host DNA millions or billions of years ago and are now inherited. The wonder of evolution is that although no organism is a complete living fossil, all are to some extent living fossils.
Some biologists speculate that mere genetic change does not translate to evolutionary change and may in fact be inversely correlated with it. A case in point is the marbled African lungfish Protopterus aethiopicus. This ancient-looking species nonetheless holds the record for the largest vertebrate genome at 133 billion base pairs. DNA mutations accumulate in a steadily ticking molecular clock that indicates how long ago lineages diverged, and even in living fossil taxa this clock ticks on unimpeded, in both coding and noncoding regions of nuclear and mitochondrial DNA, demonstrating the clear independence between molecular and morphological evolution and disproving the idea that living fossil taxa can be explained by a notable lack of genetic variation.
Why Living Fossils Look Unchanged
A mystery that has long plagued biologists is why some ancient-looking forms persist for so long without evolving into new forms. In their 2010 book Biology’s First Law, Daniel McShea and Robert Brandon claim there is an automatic tendency for diversity and complexity to increase in all evolutionary systems, such that any “static” species deserves special explanation. As a way of introducing potential explanations, consider our hominin ancestors’ Acheulean bifacial hand axes-the height of cutting-edge prehuman technology-which existed unchanged for a million years. More recently, stone points underwent rapid change. Today’s ever-changing mobile phones and other electronic devices are virtually obsolete the moment they come out of the box. Still, it took a century for engineers to improve on Thomas Edison’s original incandescent light bulb, and other inventions have survived in early form with essentially no modification, from simple chairs, pencils, and sandals to more elaborate combustion engines and lead batteries. Why have these inventions, like living fossil taxa, remained the same for so long?
Evolutionary biologist George Williams keenly noted in his 1997 book The Pony Fish’s Glow that “adaptationist stories are not about evolution so much as about its absence.” Such stories focus less on how various features arise than on why they are maintainedwhy they do not continue to evolve. Once the bipedal stance, big brains, and opposable thumbs of human ancestors arose, why did these features linger? Natural selection preserves features by preventing their loss. In describing this corrective, optimizing process of normalizing selection, Williams wrote, “What natural selection mainly does is to cull departures from the currently optimum development.” Aristotle’s descriptions of wild animals and plants, written 2,500 years ago, are still accurate for their descendants today, mainly because natural selection has prevented their evolution. Although Darwin had already one-upped Williams by noting the same thing about flora and fauna of ancient Egypt, we give Williams the final word: “To a relatively small directional residue [of genes] we attribute the great panorama of evolution.” But could a few genes explain so much of evolution?
Regardless of stabilizing selection’s importance, the fact remains that genetic change cannot be stopped. An intriguing hypothesis of “evolutionary capacitance” suggests that organisms continually build up genetic change, which is not reflected in a similarly steady increase in phenotypic variation-at least until something disturbs this pent-up potential for evolutionary transformation. Experiments on fruit flies suggest that key proteins regulating complex developmental processes, such as Hsp90 and other heat shock proteins, undergo conformational shifts during times of environmental stress, so that normally closely controlled gene expression is left unguarded, potentially unleashing a torrent of new variants in a burst of experimentation that punctuates the static equilibrium. Further studies have revealed that most genomes appear to hold phenotypic variation in check until these usually reliable regulatory proteins are functionally compromised by unfolding, allowing for genetic variation and thus key innovations to arise within populations.
It is possible, then, that living fossils are simply anomalous species that have left hidden reserves of potential phenotypic variation untapped. On the other hand, living fossils could merely be exceptions to the general rule of extinction. It is unclear how much of their longevity derives from extrinsic, ecological factors, rather than genetic factors. Surely these organisms have lessons to teach about the role that stochastic contingencies play in evolutionary history. A number of rare relicts of lineages thought to be extinct actually flourish if introduced to new areas. This ability to thrive suggests that the survival of a living fossil may have less to do with a feature of the organism itself or its specific habitat than with chance events in history, including disasters or the new arrival of predators and competitors.
Paleontologists have induced from well-studied episodes of Earth’s history that mass extinctions generally lead to wholesale replacement of flora and fauna. Ammonites, coiled-shell mollusks similar to today’s nautilus, were dominant marine predators before the rise of bony fishes. Mammal-like reptiles dominated the land until their extinction led to the rise of the dinosaurs at the end of the Triassic Period, and once dinosaurs went extinct at the end of the Cretaceous Period, mammals and birds radiated to fill many ecological niches previously occupied by dinosaurs.
Aside from the extinction of potential competitors, the evolution of a new trait can provide a key innovation that opens the door to adaptive radiation. For example, the evolution of preycatching webs in spiders spurred their tremendous success, as measured by the group’s diversity, abundance, and longevity. The acquisition of internal symbionts by detritivores, allowing them to subsist on decaying vegetation, likewise led to their widespread role as crucial elements of many ecosystems.
In the business arena, experts use the term wide moat to describe entrepreneurial plans that allow a company to gain and hold, in monopolistic fashion, a strong market share by being the first to establish a product before competition moves in. Trade names that are synonymous with products (Xerox for photocopies, Kleenex for facial tissues, Band-Aids for adhesive bandages) typically represent firms that filed patents or otherwise became initially identified with goods or services, and as such may represent the business analogue of how living fossils fend off competition.
Biologists refer to this fundamental process as competitive exclusion: Organisms defend resources and prevent potential competitors from taking over their ecological niche by evolving adaptations to exploit an available resource, forcing other species toward extinction or to another niche, so that they cannot gain leverage to reduce the original claimant’s “market share.” Perhaps living fossil taxa face little opposition “from having,” as Darwin put it, “inhabited a confined area, and from having thus been exposed to less severe competition.”
Just as wide-moat companies are good bets for investors seeking continued performance, living fossils yield strong long-term returns. Two likely explanations, again mirroring factors in the business world, might explain this cornering of the market, leading to a preemptive strike against prospecfive competitors. One is hitting on a winning formula early on; another is living in a stable, predictable environment where there is little competition for resources, which may initially be abundant. Ecological stasis might reward morphological stasis, and species that are well adapted face little need to change without the spur of an environmental alteration, leading to greater stabilizing selection.
When many animal body plans originated, forged in the crucible of the Cambrian explosion, successful evolutionary experiments left little room for new arrivals. An economist would say that all the $100 bills have already been picked off the sidewalk, or all of a tree’s low-hanging fruit harvested. Some biologists claim that living fossils are predominantly ecological generalists, giving them a competitive advantage; others argue they are typically specialists. A survey of living fossil species’ shows that both hypotheses are supported. Key innovations tilt forms toward specialization but can just as easily open up numerous possibilities, and because living fossils tend to represent ancient lineages, the innovation may be so old-an eye, a wing, or a worm-like body plan-as to be found in many organisms today. Insects, by all accounts the most successful animals in Earth’s history, can be seen as either specialized or generalized.
Isolation can be a refuge or a trap. In his 1991 book on living fossils, Keith Stewart Thomson claimed they “manage to survive only by retreating to some isolated environment where some special circumstance allows them to hang on,” but noted that if later transferred to a wider range where they are placed in direct competition with other organisms, they seldom fare well. Clearly this generalization does not always hold true. Ginkgo and dawn redwood trees now grow around the world. Many aquariums exhibit lungfishes, and African lungfish are well known for estivating in a ball of drying mud to escape prolonged desiccation, which enables them to survive dire conditions that kill other fish. These examples of adjustability suggest that it is not simply blind luck-surviving a cataclysmic extinction, or being first to move into a new niche-but often a key innovation that renders living fossils successful in persisting for long stretches of time.
Defining Species over Time
Living fossils reflect profound scientific and philosophical issues about the concept of species, which can be considered a unit of classification, of evolution, or both. Prior to Darwin, scientists imagined each species as an essential type or ideal Platonic form. Darwin showed not only that species change over time but also that they include considerable variation, which we now refer to as polymorphism, something he recognized not as a flaw but as an asset, providing a reservoir of raw material for selection. But living fossils raise troubling questions. Even as we recognize microevolutionary adaptation of shifting gene pools within species, it is hard to say how much a species changes from one generation to the next, and when a change is sufficient to mark the dividing line demarcating new species.
The philosophical problem of gradual changes leading eventually to a major change is mirrored by such quandaries as how to determine when a boiling teakettle turns from hot to cold, or a growing child from short to tall. Darwin himself was skeptical of species concepts: “I look at the term species as one arbitrarily given, for the sake of convenience, to a set of individuals closely resembling each other, and that it does not essentially differ from the term variety, which is given to less distinct and more fluctuating forms.”
As evolutionary biologists have long noted, the discontinuous human mind sees natural breaks in continuous phenomena. In Richard Dawkins’s words, names of ever-changing species are “no more than a convenient fiction, a pandering to our own limitations… Without gaps in the fossil record, our whole system for naming species would break down.” In this view, species can be seen as frames of motion picture film, frozen images representing momentary flashes of time. The concept of static species works well for any particular instant of the past or present but not for continuous stretches of deep time. Just as Heraclitus famously observed that one can never step twice into the same stream, species likewise present a conundrum for biologists. As Dawkins argues, “These are evolutionary regions into which our zoological naming conventions were never designed to go.”
A great hullabaloo surrounded the 2009 announcement of the basal primate Danvinius masillae as the “oldest human ancestor.” This public relations ploy was an absurd statement: Strictly speaking, the oldest ancestor would have to be the very first life form. Darivinius is known from a single, beautifully preserved fossil, but it lived nearly 50 million years before humans appeared. The notion of ancestors and descendants is tricky. Some systematists reject the progressive, ladder-like view of evolution (straight-line evolution known as anagenesis and orthogenesis) in which a species gradually changes into, and is replaced by, a newer species; they argue instead that every spéciation event occurs by the branching process of cladogenesis, named for the resulting branches on the evolutionary tree.
The problem with adding the axis of time to the concept of species is that we know only the anatomy of ancient fossils. Biologists long ago distinguished species solely on the basis of form. This morphological species concept proved knotty, not least because some species display so much polymorphism as to look like many rather than one unified species; other species so closely resemble each other they can scarcely be told apart. Fortunately, this scheme was eclipsed in 1942 by Ernst Mayr’s biological species concept, which distinguishes species on the basis of their inability to successfully interbreed. A consequence of this universal reproductive isolation, which can occur in many forms ranging from incompatible gametes to different mating behaviors, is not only a lack of reproductive compatibility but also some sort of discrete distinction, a clear-cut gap that separates different species, providing evidence they are not exchanging genetic information.
However, this distinction is not always anatomical and thus evident in the fossil record; it could just as easily be ecological, behavioral, biogeographic, cellular, or molecular. Mayr’s criterion of reproductive compatibility is nearly universally accepted because it works well to distinguish living species, but it applies only in the here and now. It is a purely horizontál concept, based on space but not applicable over the vertical axis of time, because ancient gene pools are inaccessible. Another important lesson offered by living fossils is the biased, selective nature of the known fossil record.
A potential solution, although an equally problematic one, is G. G. Simpson’s evolutionary species concept, which defines a species as a lineage evolving separately from others and with its own distinct role and tendencies. Some use this concept to define a species as the smallest taxon with its origin in a lineage-splitting event. These concepts are dubious, because it is hard to know what is meant by a distinct evolutionary role and tendency. Lineage-splitting events are equally difficult to define. Certainly not all populations produced by splitting lineages are equivalent, and to consider them all under one concept, the species, would be profoundly misleading.
Indeed, a notable strength of Mayr’s biological species concept is that it provides a potentially objective criterion for distinguishing species: reproductive isolation. Better still, it also gives us an explanation for why species, as reproductively isolated populations, exist in the first place. Reproductive isolation protects the suite of adaptations that fit a species to its particular environment. Any dilution by genetic information from another species would only weaken those adaptations and their integration. Thus we are thrown back on Mayr’s concept, despite its one-dimensional nature, and the difficulties in applying it to populations that do not reproduce sexually or that engage in horizontal gene transfer.
To complicate matters further, spéciation is only rarely instantaneous, as in the origin of a new species of selffertilizing plant by the doubling of its chromosome number. In most cases, reproductive isolation develops gradually and in geographic isolation. We can only be sure it has happened after the fact, when populations occupy the same regions but do not exchange genetic information. In fact, the number of cases in which reproductive isolation between species has been directly tested is very small. It is usually inferred from morphological, ecological, or behavioral distinction. Many recent studies reveal these distinctions may not be obvious. What appear to be morphologically and ecologically uniform populations may comprise reproductively isolated subgroups whose presence is seen only when sequences of their genomes are studied.
If current theories of spéciation are accurate and reproductive isolation continues as the heart of biology’s dominant species concept, any attempt to apply it over time is futile. If we were able to trace the ancestry of the horseshoe crab back generation by generation to its Ordovician ancestors, we could not define points at which one species directionally became another. Yet we can be quite confident that today’s horseshoe crabs are reproductively isolated from their ancestors, although connected to them by a seamless thread of parent-offspring relationships. As biologists peer further back in time, we become less certain and finally must admit that we cannot apply species concepts with any reliability.
Despite the insuperable endeavor to define species over time, we do not deny the reality of the species category, nor do we advocate for the Darwinian view that species and varieties are simply part of a continuum. Applied without reference to a time dimension, the species category has at the very least heuristic value, because it acknowledges ecological reality, allowing biologists to catalog living things and thereby have a filing system under which we can conserve any and all information about such populations.
Living fossil taxa have much to teach us about evolutionary processes and products. They offer a stark reminder of the problems with species concepts. However, evolution is an ongoing process, not merely a historical one. Not only does evolution document life’s chronology, but it also explains the mechanisms whereby countless species have for billions of years arisen, changed, and gone extinct. Despite their apparent resistance to change, living fossils, like all organisms extant and extinct, serve as proof that evolution continues unabated as the driving force behind the tremendous diversity of life on Earth, in the past as well as in the present.