Diseases and the Evolution of Pathogens

One of the basic premises of this book is that Cretaceous insects transmitted pathogens that either directly or indirectly affected dinosaurs. The results were not only dinosaur disease and mortality but also the destruction of dinosaur food plants. We feel that most, if not all, present-day vector-pathogen associations were already established or arose at some point in the Cretaceous, even though different genera and species of hosts and vectors were involved.

The origins and coevolution of pathogens with their vectors and plant or animal hosts are complex. When the first dinosaurs walked the earth, they already came with pathogens carried over from their ancestors. While new vector-pathogen associations were evolving, the basic survival plan of many pathogenic microorganisms had already been established.

People are in contact with microbes from the day they are born. Each of us is a walking, breathing ecosystem carrying around thousands of organisms on and in our bodies. It is said that an individual has more bacteria in his or her mouth than there are people on the surface of the globe.66 And unfortunately, sometimes we pick up pathogenic microbes.

The number of human lives lost from infectious diseases throughout recorded history far exceeds deaths from famines and war together. Epidemics have destroyed armies, wiped out indigenous peoples, halted human enterprises, and inflicted untold misery. And if not for drugs, insecticides, vaccinations, and our ability to understand the causes of diseases and act accordingly, our current census figures would be much lower. How many more of our species would have died from malaria and yellow fever if we had not cleared the land, drained the swamps, used tons of pesticides, and built dwellings with screened windows? Yet even with all of this, yearly mortality rates from just malaria are well over a million. What role did diseases play in regulating the distribution of animals and plants in ancient landscapes?

Vertebrate diseases are commonly lumped into two categories, contagious and noncontagious. In contagious illnesses, the pathogens are spread from one individual to another by direct or indirect contact. Touching the infected individual, breathing the same air, coming in contact with contaminated waste products, and so on all serve to spread the infectious agent. On the other hand, noncontagious diseases need to be passed on by another organism, commonly known as a vector, that inoculates the pathogen into the host. Just coming into contact with sick individuals will not result in infection. We have shown that vector-borne pathogens existed in the Cretaceous. However, evidence of contagious diseases has not been discovered, although they were certainly present back then. Especially lethal representatives of both types of diseases have been considered for use as biological weapons.262

In general, epidemics causing widespread mortality originate in two ways. Either a pathogen already present in the ecosystem mutates into a more lethal strain or an already existing pathogen makes contact with a new, exotic host. An example of the former would be the bird flu virus that has developed strains capable of infecting humans. Instances of the latter were the introduction of smallpox and measles into the New World and their widespread destruction of Amerindian populations. Perhaps the most dangerous situations are those that combine both features, that is, a newly introduced, actively mutating pathogen.

So when and how did pathogens arise? Scientists believe that the precursors of life arose in primordial oceanic ooze as simple organic molecules that polymerized into complex amino acids, the building blocks of life. These were incorporated into abiotic protocells, and when nucleic acids were manufactured in that generative cauldron, true cells were formed. Those very first pre-life forms were probably similar to two unusual pathogens. The simplest of these are the prions, which are composed only of a single protein. Viroids are more complex and are made up of a short chain of naked RNA. Their elementary structure suggests that these were the most ancient pathogens.263 264

Following along with this line of thinking would mean that the first diseases probably occurred in bacteria. These prokary-otes, cells without nuclei and most organelles, first appeared as fossils 3.5 billion years ago. They then had 2 billion more years to experiment with diversification and develop complex metabolic pathways. During this interval, viral pathogens such as bacterio-phages had sufficient opportunities to arise, invade, and coe-volve with bacteria, thus establishing one of the earliest disease associations.

By 1.5 billion years ago, fossil eukaryotes—organisms with well-defined nuclei and organelles—arrived on the scene. There is good evidence that two of these organelles, mitochondria and chloroplasts, represent small symbiotic bacteria that pushed their way into larger eukaryotic cells and remained. This would be extremely significant if it meant that the invasions of en-dosymbionts were responsible for the critical transition from prokaryotic to eukaryotic life. After all, in order to function, the majority of all life on earth depends on mitochondria, and the plants that form the basis of our food chain require chloroplasts! There is data showing that mitochondria from higher plants are so different from that of all other eukaryotes that their invasion had to have taken place on a separate occasion. This means that at least three different symbionts were able to gain permanent entry to primitive cells. Furthermore, the first eukaryotes were probably protists, and many of these are known to be hosts to en-dosymbiotic bacteria as well as to other smaller protists. If one accepts that these mutualistic associations were present, than why not parasitic ones as well? The same invasive mechanisms could easily have worked for both beneficial and detrimental symbionts. Most pathogenic microorganisms, as well as meta-zoan parasites, evolved from free-living ancestors that lived as saprophytes, predators, or ectoparasites of other organisms.

Over eons, viruses, bacteria, fungi, protozoa, and nematodes formed endosymbiotic associations with higher life forms, including vertebrates. As pathogens experimented using the vertebrate body for food and shelter, they elicited various responses in the host, the most drastic being death. Each infected animal developed ways to combat these invaders. Just when immune responses appeared in eukaryotes is unknown, but at some point vertebrates developed an arsenal of general and specific defensive weapons to use against foreign bodies. The first line in a general defense is a protective integument to keep the organisms out. However if this barrier is broken or entry occurs through the digestive or respiratory systems, blood cells then may engulf and destroy the parasites. Protective proteins, including complement and interferon, also battle the intruders. When this doesn't work, a more specific battle is mounted and an immune response triggered by antigens on the surface of the invaders stimulate the production of antibodies. If the host survives that first contact, it has an acquired immunity towards that pathogen, which may be complete or only partial.265

When the immune system is overwhelmed or compromised from dealing with too many infections, the host may perish. Whether a vertebrate can survive an infection depends on the number of parasites introduced (the infective dose), the immune system response (whether there was previous exposure), and environmental conditions.266 Throughout recorded history, deadly epidemics in humans were often caused by pathogens not previously experienced. These "novel" or "emerging" pathogens are usually mutated strains of existing organisms or the transfer of disease-causing agents from reservoir animal hosts (zoonosis).

What kind of resistance to disease did dinosaurs have, and is it possible that their immune systems were not prepared for certain pathogens? Were dinosaurs unable to produce the antibodies crucial in defending them against protozoan and viral pathogens?267 There is some evidence of pathogens and parasites associated with dinosaur fossils. Aside from the presence of gastrointestinal parasites in dinosaur coprolites135 (color plates 16B, 16C, 16D), some observations might pertain to infectious microbes in dinosaur blood vessels. In a microscopic preparation of a sauropod bone from Wyoming, Moodie268 observed ovoid bodies around the periphery of the vascular spaces. While some of these bodies resembled reptilian blood cells, others were irregular and appeared to be agglutinated corpuscles. Roy Moodie mentioned that similar small, round bodies had also been observed in the Haversian canals of an iguanodon. Is it possible that some of these were infectious microorganisms? A more recent study showed putative blood cells in a vessel of a T. rex containing diffuse gray bodies, which may represent developmental sites for malaria or leishmanial parasites.269

Today, most vector-borne infectious diseases occur in tropical or subtropical climates, which suggests that pathogens, hosts, and vectors originated under similar conditions. During the Cretaceous, when we propose that vectors and pathogens were coe-volving, the climate was predominately tropical to subtropical.180


As mentioned earlier, viruses are assumed to be quite ancient and their first hosts were likely bacteria. There are several hypotheses on virus origins, one of which states that they extend back to the beginning of life some 3.8 billion years ago. This seems plausible and would give viruses an extended period to invade higher life forms as they appeared on the scene. Today some 1,950 species of viruses have been described from a wide range of plants and animals.272 The origins of various lines have been estimated using molecular techniques. While those methods can estimate when various lineages arose in the past, it is still good to have fossils to confirm the time and place. As would be expected, the fossil record of viruses is virtually nonexistent, except for putative cytoplasmic and nuclear polyhedrosis viruses in adult biting flies in Burmese amber.172 Indirect evidence of polydna viruses is found with fossil braconid wasps, whose present-day counterparts utilize these viruses to suppress host immune reactions (color plate 13A). Discovery of these insect viruses provided evidence to support the hypothesis that some arthropod-borne viruses (arboviruses) evolved first as pathogens of bloodsucking flies. This seems plausible since several groups of viruses such as the Togaviridae, Reoviridae, Poxviridae, and Rhabdoviridae have members that can infect both insects and vertebrates.271 This dual-host biology is also seen with viruses that infect both insects and plants and illustrates the wide cross-phyla host range of many viruses. It is likely that not only ar-boviruses but also other contagious viruses infected vertebrates throughout the Cretaceous. Whether they caused disease in dinosaurs cannot be said, but we know that the vectors that transmit them today were also present back then. Many of the insect groups that transmit plant viruses today were also present at that time, and while viruses from angiosperms abound, very few have been observed in other plant groups. Plant viruses were certainly important in defining community structure then as they are now.


We have already spoken about the early evolution of the ubiquitous bacteria, of which some 10,000 species have been described so far. Fossils demonstrate that they began evolving in the oceans 3.5 billion years ago. Our knowledge of the planet's prokaryotes is extremely limited even though they are so numerous that only a milliliter of water typically contains up to a million bacteria. Being so widespread, it is not surprising that some are transferred from the mouthparts of horseflies, lice, ticks, and sand flies to vertebrates. We've discussed bacteria carried by arthropods, but other types known as facultative pathogens may have been equally important. These include the cosmopolitan pseudomonads and serratias that enter wounds and spread throughout the circulatory system, cleverly avoiding immune re-sponses.234 If dinosaurs had been contaminated via wounds, resulting infections could have been fatal, much as they are in lizards killed by Serratia today.270

A number of other bacteria, similar to those that cause strep throat, pneumonia, tuberculosis, and diarrhea in humans, are acquired by inhalation or via contaminated foods or liquids. These organisms, as well as anthrax that occurs worldwide in populations of wild and domestic vertebrates (also occasionally man) and is spread through cuts, abrasions, and inhalation, were probably circulating among Cretaceous vertebrates. Some of these communicable organisms could have presented serious threats to dinosaurs.


Rickettsias are minute rod-like organisms often considered bacteria. They occur in many locations inside the alimentary tract and tissues of a wide variety of animals. Some cause diseases in insects,271 while others are pathogenic to both arthropod vectors and their vertebrate hosts. Symbiotic species in the wide-ranging genus Wolbachia play various beneficial roles in arthropods, even digesting portions of the blood meal in biting insects. The fossil record of rickettsia is non-existant and few scientists have described these very small organisms because they are difficult to culture. Two serious human rickettsial pathogens are those that cause the plague, transmitted by fleas, and typhus, carried by lice. Rickettsia certainly resided in dinosaurs, but whether they resulted in epidemics cannot be answered.


There are over 100,000 species of fungi273 and they have established relationships with all life forms. At least 77,000 different plant-fungus associations occur in just the United States,274 so if we consider those on the rest of the globe and also include the fungal pathogens of invertebrates and vertebrates, as well as those living in the soil, freshwater, and the sea, their overwhelming presence becomes obvious. The earliest fossils date back some 460 mya to the Ordovician period, and by the Devonian, terrestrial plants were being invaded by fungi.273 There are even reports of fossil fungi in ancient Araucarioxylon wood, thus providing some credence to our scenario of Cretaceous wood-boring insects transmitting plant-pathogenic fungi in those ancient forests. Fossils of bark and long-horned beetles dating from that time further support this scenario. Other gymnosperms could have lost their leaves from fungal attacks, since epiphyllous types growing on conifer leaves also existed in that period. Moreover, fossils show that by the mid-Cretaceous, mushrooms were quite abundant (color plate 12D),345 as well as fungal parasites such as one infecting a scale insect in Burmese amber (color plate 13D).

Aside from affecting dinosaurs indirectly by destroying their plant food sources, fungi could have infected and even killed hatchlings, just like they do to reptiles today.275 Many of these fungi belong to common soil genera (Aspergillus, Mucor, Cephal-osporium, Penicillium, Beauveria, and Fusarium) that either grow on the skin or lodge in the respiratory and digestive systems. One species of Beauveria is known to kill alligators,276 and since this genus also attacks insects, it is possible that arthropods mechanically transmitted the spores. Certainly the most lethal infections to dinosaurs would have been those that became established in their respiratory systems and caused mycotic pneumonia.


Protozoa, with some 65,000 described species, are an ancient group with a fossil record extending back to the Archean Eon, some 2 billion years ago. While the earliest forms were certainly free-living in the sea, feeding on bacteria, algae, and one another, it didn't take long for them to establish symbiotic associations with other life forms. Their first relationships were proba bly simple attachments to the body wall of organisms living in the same aquatic environment (ectophoresis). At one point in time, they developed ways to burrow into the skin of their carrier, obtaining nourishment and becoming ectoparasites. Later on, different types invaded the alimentary tracts of animals, just living there and feeding on partially digested food (endophore-sis). Many of them, especially the flagellates, became permanently established in the guts of insects, especially in termites where they play an important role in digesting the cellulose (or in carrying around internal organisms that do the job). Additional protozoa, especially the ciliates and coccidians, penetrated into the body cavity of their animal hosts, multiplying mostly by simple division and forming resistant stages (cysts) between hosts. Eventually those that lived in bloodsucking insects were transported into vertebrates, became established, and caused serious diseases. Curiously, very few protozoa, aside from species in the genus Phytomonas, formed any continuous associations with plants.

Two important groups were present in the Cretaceous, malarial organisms and trypanosomatids, and fossils show that they have existed for at least 100 million years. Malarial parasites of the family Plasmodiidae consist of ten genera, the best known being Plasmodium, which infects reptiles, birds, humans, and other mammals throughout the world.280-282 While related to coc-cidian parasites, it is difficult to trace them back to any free-living ancestral group. One Tertiary fossil record of Plasmodium plus one Cretaceous record shows that malarial organisms had already evolved their complicated life cycle millions of years ago.167'283

The life cycle of these protozoans has become very intricate and involves multiple stages. The vector acquires pre-sexual stages of the parasite from the blood of infected vertebrates. After undergoing sexual maturity in the insect, the malarial organism develops into a cyst that eventually becomes filled with minute thread-like bodies called sporozoites. Upon their release, the motile sporozoites migrate through the arthropod's body cavity and enter the salivary glands, where they are transferred back to the vertebrate at the next blood meal (fig. 23).

The four types of malaria infecting humans all belong to the genus Plasmodium, which also infects monkeys and the higher apes. Malaria caused by species of Haemoproteus, considered to be the most primitive type, is spread by biting midges and occurs in birds, reptiles, and amphibians. This type of malaria was discovered in Burmese amber.167 What is difficult to establish is just when biting midges started transmitting these vertebrate pathogens. Since the earliest known biting midge fossils occur in Lebanese amber, and some of these have mouthparts adapted for biting vertebrates, disease transmission could have occurred by that period. Because the effects of these organisms on extant reptiles are poorly known, we can only compare their possible effects on dinosaurs from our knowledge of human malaria, which can be quite devastating.

Flagellates of the family Trypanosomatidae, which were also discovered in Burmese amber, include those responsible for sleeping sickness and leishmaniasis. The motile stages have a fla-gellum emerging from their anterior end and do not differ significantly in appearance from their supposed free-living ancestors, the euglenoids. The first stage toward parasitism in this group was probably the establishment of colonies in the guts of animals living in the environment. The original hosts may have been marine nematodes, followed by soil and freshwater roundworms. Those trypanosomatids that did eventually colonize the gut of bloodsucking insects such as sand flies could have evolved into the vertebrate-pathogenic leishmanias.346

Recent studies indicate that parasitic lines evolved at least four times with these protozoa.285 286 This is obvious because the fish and amphibian parasitic trypanosomatids vectored by leeches certainly arose independently from those carried by sand flies to mammals and lizards. While the origin of infectious trypanoso-matids is controversial, with some suggesting they arose in ver-tebrates,284 sand flies possibly obtained the parasites originally from plants infected with Phytomonas. The discovery that female sand flies imbibe plant secretions and Leishmania produces cellulose-degrading enzymes287 supports a plant-origin hypothesis for at least one of these lines. All we can be certain of is that sand fly-vectored trypanosomatids infected reptiles 100 mya.

If these vector associations were newly established in the Early Cretaceous, the effect of trypanosomatids on vertebrates could have been devastating. Possibly the dinosaurs were one of the original host groups for these "emerging" pathogens, which often have a severe impact on their hosts.288 Both Trypanoplasma and Trypanosoma are transmitted to fish by leeches. Because of a long association with their hosts, species of Trypanosoma are no longer lethal to the fish. However, species of Trypanoplasma, which are regarded as emergent pathogens that only recently (evolutionary speaking) began infecting fish, can inflict debilitating illness and death. During the early stages of coevolution, sand fly-transmitted trypanosomatids could have behaved like Trypanoplasma and caused rampant infections, epidemics, and deaths.


Of the approximately 20,000 described nematode species, over 6,000 live in vertebrates, about 4,000 are associated with invertebrates, and 3,000 or more are plant parasites.173 277 278 The remainder are free-living in soil, fresh water, and salt water. At least 39 species parasitize humans, 46 occur in dogs, and 32 in cats. The tissue specificity of nematode parasites is apparent when examining their locations in cats; different ones are found in the colon, stomach, small intestine, kidneys, lungs, heart, spinal cord, lymph vessels, diaphragm muscles, and even the middle ear.279 Reptiles and amphibians share many more genera of parasitic nematodes than reptiles and birds or reptiles and mammals, suggesting that body temperature is an important factor in host selection.

Nematodes inhabit all possible niches, from deep-sea trenches to the placenta of whales. The earliest described fossils are mer-

mithid parasites of insects dating from the Early Cretaceous (color plate 13C), but other fossils extend back to the Devonian. Ancient marine roundworms probably swarmed through the oozes bordering Cambrian seas since those inhabiting marine and freshwater habitats today represent the most primitive lineages. Nematodes presumably adapted to terrestrial habitats by the Silurian, some 420 million years ago. These free-living forms could have easily shifted their diets from marine to freshwater and soil microbes, ultimately invading available niches in plants, invertebrates, and vertebrates. Curiously, many did not give up their early dependence on bacteria, and the first animal parasites were probably pinworms (Oxyurida) that feed on bacteria in the alimentary tract of invertebrates and vertebrates. Other parasites (Strongylida) switched to a fluid diet in the vertebrate alimentary tract, but the free-living juveniles still feed on soil bacteria before they enter the host. Some nematodes, such as those in the insect-parasitic genera Steinernema and Heterorhabditis, solved their dependency on bacteria by introducing specific species of soil bacteria into their hosts. The bacteria multiply and kill the insects, at the same time providing the worms with a food source inside a protected microenvironment.279

Nematodes continued to coevolve with their plant, invertebrate, and vertebrate hosts, probably establishing parasitic relationships soon after their hosts appeared. The stomach worms (ascarids) were extremely successful in severing their dependency on bacteria. Aside from infecting over a billion humans as well as other mammals, ascarids also parasitize sharks, fish, amphibians, reptiles, and birds279 (fig. 32). They even parasitized dinosaurs135 (color plates 16C, 16D).

Two separate lines of vertebrate parasitic nematodes, the spiru-rids and filarids, use arthropod vectors to reach their hosts.173279 Filarids develop in the tissues of their hosts and produce special micro-larvae (microfilaria) (fig. 31) that are picked up when the vectors take a blood meal. In contrast, spirurids live in the alimentary tract of vertebrates. Their eggs are voided with the feces and hatch when eaten by various beetles and orthopterans. The roundworm's future depends on a vertebrate choosing the parasitized insect for lunch. A large number of vertebrate parasitic nematodes occur throughout the world today, and some of those whose ancestors could have parasitized dinosaurs are discussed in the chapter on parasitic worms.

We know essentially nothing about plant-parasitic nematodes of the Cretaceous world. But be assured that they were just as common as they are at present and attacked the roots and in many cases the stems and leaves of representatives of all the diverse floral groups that thrived during that period.

So just how badly did dinosaurs suffer from parasites? Based on what we know regarding pathogens of reptiles and birds and when the various groups appeared in the past, dinosaurs were susceptible to oral sores caused by bacteria, trematodes, and ne-matodes, lesions in their esophagi from kalicephalid nematodes, stomach wounds from spirurid and ascarid nematodes, and intestinal damage from capillarid nematodes, Ophiotaenia tapeworms, and amoeboid protozoans. Their internal tissues probably contained trematodes and filarial nematodes, and their muscles tapeworm larvae (plerocercoids) and nematodes. The blood vessels, especially those around the heart, in all likelihood were filled with filarial nematodes. Microfilaria undoubtedly circulated through their veins, and malarial and leishmanial parasites developed in their blood cells. Perhaps their lungs were filled with protozoans and lungworms and their spleen and liver contained malarial and leishmanial pathogens. Even their fat tissue conceivably hosted trematode larvae and protozoans. In addition, fly larvae could have developed in their nostrils as well as around scratches or wounds. And lastly, a plethora of viral and fungal diseases certainly were responsible for everything from pneumonia and diarrhea to death. This would have been the worst scenario.

Diseases can be very important controlling factors of animal populations, although they are often overlooked.66 Parasites affect their host in many ways, from behavioral and physical changes to a reduction of fecundity, and finally death. There is ample evidence that vector-borne diseases can inflict high mortality levels, especially if they recently, geologically speaking, appeared on the scene like some human forms of malaria. If sand flies first established vector relationships with trypanosomatids, and biting midges with haemoproteans, in the Early Cretaceous, then these new diseases definitely were capable of threatening the very existence of dinosaurs. Even if some were able to tolerate full-blown infections, other stress factors such as starvation or additional parasites would have upset their equilibrium and led to death.

Global epidemics potentially occurred as infected sand flies, biting midges, and dinosaurs dispersed and expanded their range. Pandemics possibly spread between Asia and North America via the Beringia land bridge, which was present by the Late Cretaceous.289 Since arthropod carriers were undoubtedly universally distributed at that time, the disease cycle continued no matter where dinosaurs lived. Further distribution of diseases between and in North and South America became possible through Central America in the latest Cretaceous.290 Infected insects then as now were dispersed by wind currents, and mosquitoes and midges have been collected at altitudes from 5,000 to 13,000 feet.291 At such heights, intercontinental dispersal of pathogen-bearing insects becomes a definite possibility.

Just as we now fear flu viruses that can be introduced by migrating birds and then "jump" to humans, the same scenarios were probably happening in the Cretaceous with other diseases.

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